How do landscape composition and configuration, organic farming and fallow strips affect the diversity of bees, wasps and their parasitoids?

Authors


*Correspondence author. E-mail: a.holzschuh@agr.uni-goettingen.de

Summary

1. Habitat destruction and increasing land use intensity result in habitat loss, fragmentation and degradation, and subsequently in the loss of species diversity. The fact that these factors are often highly confounded makes disentangling their effects extremely difficult, if not impossible, and their relative impact on species loss is mostly speculative.

2. In a two-year study, we analysed the relative importance of changed landscape composition (increased areas of cropped habitats), reduced habitat connectivity and reduced habitat quality on nest colonization of cavity-nesting bees, wasps and their parasitoids. We selected 23 pairs of conventional and organic wheat fields in the centre of landscape circles (500 m radius) differing in edge densities (landscape configuration) and % non-crop habitats (landscape composition). Standardized trap nests were established in the field centres and in neighbouring permanent fallow strips (making a total of 92 nesting sites).

3. Factors at all three scales affected nest colonization. While bees were enhanced by high proportions of non-crop habitat in the landscape, wasps profited from high edge densities, supporting our hypothesis that wasps are enhanced by connecting corridors. Colonization of herbivore-predating wasps was lower in field centres than in fallow strips for conventional sites, but not for organic sites, indicating a fallow-like connectivity value of organic fields. The relative importance of habitat type and farming system varied among functional groups suggesting that their perception of crop–non-crop boundaries or the availability of their food resources differed.

4. Local and landscape effects on parasitoids were mainly mediated by their hosts. Parasitism rates were marginally affected by local factors. A specialist parasitoid was more sensitive to high land use intensity than its host, whereas generalist parasitoids were less sensitive.

5. We conclude that the conversion of cropland into non-crop habitat may not be a sufficiently successful strategy to enhance wasps or other species that suffer more from isolation than from habitat loss. Interestingly, habitat connectivity appeared to be enhanced by both higher edge densities and by organic field management. Thus, we conclude that high proportions of conventionally managed and large crop fields threaten pollination and biological control services at a landscape scale.

Introduction

Habitat loss, habitat fragmentation and degradation of habitat quality are considered to be among the main threats of biodiversity (Harrison & Bruna 1999; Fahrig 2003). While habitat loss or the amount of remaining habitat types within a landscape are measures of habitat area independently of the configuration of habitat patches (landscape composition), habitat fragmentation is a measure of connectivity which is strongly affected by the geometry of habitats (landscape configuration) (Fahrig 2003). Linear habitat strips which connect otherwise isolated habitats can enormously reduce habitat fragmentation even if the total area of habitat strips is low (Haddad & Tewksbury 2005). Knowledge of the relative importance of habitat loss, fragmentation and degradation is essential for understanding changes in diversity and species interactions, and for implementing effective conservation and restoration measures (Collinge 1996; Fahrig 1997). However, the separation of effects of habitat loss and habitat fragmentation has frequently proved difficult in real landscapes, because both factors are often highly confounded (Fahrig 1997; Trzcinski, Fahrig & Merriam 1999; Debinski & Holt 2000; Cushman & McGarigal 2003; Ritchie et al. 2009). Furthermore, habitat fragmentation often results in the degradation of habitat quality in the remaining patches and consequently impedes the disentangling of landscape and local factors (Harrison & Bruna 1999; McGarigal & Cushman 2002; Fahrig 2003). The aim of our study was to examine the relative importance of landscape composition, landscape configuration and local habitat quality which was influenced by land use intensity. Agricultural landscapes can be ideal study environments for disentangling such effects. This is the case, if the length of connecting non-crop strips such as field banks and margin strips (a measure of configuration) is independent of the total amount of non-crop habitat (a measure of composition) across landscapes, and if habitats differing in local quality occur across all landscapes.

To date, effects of landscape composition and connectivity have almost always been examined separately. The positive impact of landscape connectivity is known from studies on habitat corridors which connect otherwise isolated habitat patches (e.g. Haddad 1999; Baum et al. 2004). In agricultural landscapes, grass strip corridors in a crop field matrix enhance the colonization of new nesting sites by wasps (Holzschuh, Steffan-Dewenter & Tscharntke 2009). However, studies on the effects of corridors in open landscapes are rare and the majority suggests that the benefits of corridors might be small compared to the impact of the quality of the remaining habitat patches and of the surrounding matrix (Öckinger & Smith 2008). Studies examining the effects of both landscape and local scales have focused predominantly on landscape composition rather than configuration and suggested that heterogeneous agricultural landscapes with many and diverse non-crop habitats enhance farmland species more than local differences in farming intensity (Kremen et al. 2004; Bengtsson, Ahnström & Weibull 2005; Clough et al. 2005). Landscape and local effects can also interact: benefits of low-intensity farming were small in landscapes with many non-crop habitats, but great in landscapes dominated by crop fields (Roschewitz et al. 2005; Rundlöf & Smith 2006; Holzschuh et al. 2007; Rundlöf, Nilsson & Smith 2008). However, local increases in land use intensity have often been found to affect species diversity enormously. Conventional farming reduces diversity and abundance of a range of taxa compared to organic farming (reviewed in Bengtsson et al. 2005; Hole et al. 2005), and diversity and abundances are lower in field centres than in field edges, field margins or fallow strips (Fussell & Corbet 1991; Bäckmann & Tiainen 2002; Marshall & Moonen 2002; Pywell et al. 2005; Clough et al. 2007). Here, we assess at once the impact of two local factors (farming system and habitat type), of landscape composition and of landscape configuration.

The perception of landscape, habitat type and farming intensity may strongly differ among species, functional groups and trophic levels, resulting in changed species interactions (Tscharntke & Brandl 2004; Diekotter et al. 2007). Higher trophic levels such as specialized parasitoids have often been hypothesized to be more sensitive to habitat loss and fragmentation than their hosts, because they have to find habitat patches which are occupied by a host, whereas their hosts only have to find a habitat patch (Kruess & Tscharntke 1994; Holt et al. 1999). Differences in the sensitivity of parasitoids and hosts may result in a release of parasitism in dependence on habitat or landscape quality (Kruess & Tscharntke 1994; Roland & Taylor 1997).

The purpose of our study was to examine how habitat type and farming intensity at the local scale, and landscape composition and configuration at the landscape scale affect nest colonization of cavity-nesting bees and wasps, and their parasitoids. Additional analyses were performed for the two functional groups of herbivore-predating and spider-predating wasps, for the dominant bee species Osmia rufa and other bee species, and for the corresponding parasitoids. All cavity-nesting bees and wasps depend on nesting sites in non-crop habitats, but forage in multiple habitats including crop fields. We established standardized nesting sites in organic and conventional wheat fields and adjacent perennial fallow strips. In a hierarchical design, we analysed effects of landscape configuration and composition (gradients of edge density and proportion of non-crop habitats in landscape circles with 500 m radius), farming system (organic vs. conventional field management) and habitat type (highly disturbed field centre vs. permanent fallow strip) on nest colonization of wasps, bees and their parasitoids and on parasitism rates.

We tested the following hypotheses:

  • 1 Nest colonization by bees and wasps increases with increasing proportion of non-crop habitats (landscape composition) and with increasing edge density providing connectivity (landscape configuration).
  • 2 Nest colonization by bees and wasps is higher in fallow strips than in field centres and higher under organic than under conventional farming methods.
  • 3 Parasitoids are more affected by agricultural intensification at local and landscape scales than their bee and wasp hosts.

Materials and methods

Study region and study sites

The study was conducted in 2003 and 2004 in 46 winter wheat fields and adjacent permanent fallow strips in the area surrounding Göttingen, Lower-Saxony (51°32′00″ N 009°56′00″ E). In the study region, very intensively used and fertile soils in flat parts of the region, alternate with less intensively used agricultural landscapes in hilly parts. Wheat is the most important arable crop in the study region as well as in most agricultural regions in Germany (Statistisches Bundesamt 2004).

Within the region, 12 study areas were selected to encompass landscape gradients from crop-dominated to non-crop-dominated landscapes and from low to high edge densities. Within each study area, a pair of organic and conventional winter wheat fields was selected for each year. As a result of crop rotation, field pairs within a study area were not the same in 2003 and 2004. In total, 23 field pairs in 12 study areas were used, because no wheat fields were managed organically in one of the study areas in 2004. Organic farmers managed wheat fields according to the European Union regulation 2092/91/EEC, which prohibits the use of synthetic fertilizers and pesticides. Instead of synthetic fertilizers, organic farmers applied animal and green manure and included legumes in the crop rotation for replenishing the soil resources. Weeds were managed mechanically or by effective crop rotations.

Each organic field was paired with the first nearby conventional winter wheat field for a comparison of farming systems which controlled for differences in abiotic conditions and landscape context. Distances between fields within a pair ranged from 0 to 600 m and between study areas from 3 to 43 km. Mean field size was 4·5 ± 0·5 ha (SE) and did not differ between the two farming types (anova: F = 2·6, P = 0·118, n = 46).

One side of each field was flanked by a permanent fallow strip between the field boundary and a farm track. Fallow strips were older than 20 years, had a naturally developed herb and grass layer, and mostly included a narrow ditch. The occurrence of a ditch and the management (mowing) of fallow strips did not differ between strips adjacent to organic and conventional fields. Mean fallow strip width was 3·0 ± 0·2 m (SE) and did not differ between fallow strips adjacent to conventional or organic fields (anova: F = 1·1, P = 0·309, n = 46).

A standardized nesting site was established in the centre of each field and each fallow strip (altogether 92 nest sites: 23 field pairs × 2 farming systems × 2 habitat types). In conventional fields, farmers did not apply insecticides within a 15 × 15 m quadrate with the nesting site in the centre. Diversity of flowering plants and flower cover were higher in organic than in conventional sites, and higher in fallow strips than in field centres (linear mixed-effects models: all P < 0·001, Table 1).

Table 1.   Mean (±SE) number of flowering plant species and % flower cover in organic and conventional fields, and adjacent fallow strips
SiteFlowering plant speciesFlower cover (%)
Conventional field centre1·7 ± 0·4<0·1 ± 0·1
Organic field centre8·1 ± 0·61·6 ± 0·6
Conventional fallow strip12·5 ± 1·50·7 ± 0·2
Organic fallow strip17·4 ± 1·31·8 ± 0·4

Trap nest communities

Standardized nesting sites (trap nests) enabled us to study nest colonization of cavity-nesting bees, wasps and their parasitoids under standardized nest site conditions (Tscharntke, Gathmann & Steffan-Dewenter 1998). Trap nests were composed of two trap nest tubes fitted on a wooden pole at a height of 1·0–1·2 m and shaded by a 41 × 50 cm chipboard roof. Each trap nest tube consisted of 150–180 20 cm long internodes of common reed Phragmites australis, which were put into a 10·5 cm diameter plastic tube. The diameters of reed internodes ranged from 2 to 10 mm. Trap nests were in the field from mid-April until harvest end-July. In the laboratory, all reed internodes containing nests were opened. For each nest, the genus of bee or wasp larvae, the number of brood cells and the occurrence of natural enemies were recorded (Tscharntke et al. 1998). Most larvae of bees, wasps and natural enemies were identified to the species level. All nests were reared separately to get the adults of bees, wasps and their natural enemies for final species identification. In some cases, no adults emerged or all brood cells were parasitized, so that only the genus (or the family in case of the eumenids) could be identified. These reed internodes were included in the analyses as additional species, if no other species of this genus (or family) was found in the same trap nest. If another species of this genus (or family) was found in the same trap nest, the unidentified species was assumed to be the same as the identified species.

Species richness represented the total number of species, abundance the total number of brood cells of bees, wasps and natural enemies from four trap nests per study site. The mortality rate was the number of parasitized or predated brood cells divided by the total number of brood cells per study site. Additionally, we performed separate analyses for herbivore-predating wasps and spider-predating wasps (Table 2), and for the dominant red mason bee O. rufa (96% of bee brood cells) and ‘other bees’.

Table 2.   Trap-nesting species, their larval food and their parasitoids. Data are from 92 trap nests in organic and conventional wheat fields and the adjacent fallow strips. Braconidae, Ichneumonidae and Acari were not further identified
GroupFamilyLarval foodSpeciesNatural enemies
Predators of herbivoresEumenidaeCaterpillarsAncistrocerus gazella, A. nigricornis, A. parietinus, A. trifasciatus, Symmorphus crassocerus, S. gracilisChrysis ignita, Melittobia acasta, Megatoma undata, Braconidae, Ichneumonidae
Predators of herbivoresSphecidaeAphidsPassaloecus corniger, P. gracilisChrysis ignita, Melittobia acasta, Megatoma undata, Ichneumonidae
Predators of spidersSphecidaeSpidersTrypoxylon clavicerum, T. figulus,Chrysis cyanea, Chrysis ignita, Megatoma undata, Melittobia acasta, Braconidae, Ichneumonidae
Predators of spidersPompilidaeSpidersDipogon intermedius
Osmia rufaMegachilidaePollenOsmia rufaAnthrax anthrax, Cacoxenus indagator, Megatoma undata, Monodontomerus obsoletus, Trichodes apiarius, Acari
Other beesMegachilidaePollen, nectarChelostoma florisomne, Hylaeus communis, H. confusus, Heriades truncorum, Megachile versicolor, Osmia leaianaChrysis spp., Megatoma undata, Melittobia acasta, Trichodes apiarius Ichneumonidae

Landscape context

For each wheat field, the surrounding landscape was characterized in a landscape circle with the field in the centre and a radius of 500 m. The radius was chosen according to the results of previous studies on trap-nesting bees and wasps (Gathmann & Tscharntke 2002; Steffan-Dewenter 2002). During field inspections, we mapped the land use in these landscape circles on the basis of official topographical maps (DGK 1:5000) in 2003 and 2004. The edge density (total length of patch edges divided by total area) and the proportion of non-crop habitats [(total area−crop field area)/total area] in each landscape circle were calculated for each year using Geographic Information Systems (GIS; Topol 4·506, Gesellschaft für digitale Erdbeobachtung und Geoinformation mbH, Göttingen, Germany and ARC/View 3·2., ESRI Geoinformatik GmbH, Hannover, Germany). We considered all interfaces between different habitat types, between crop fields cultivated with different crops, and between grassland parcels or crop fields managed by different farmers as patch edges. The edge areas of managed habitats were characterized by less intensive management than the field centres (Clough et al. 2007). The interface between crop fields or grasslands consisted of a small strip of bank vegetation. At least one of the edges of crop fields or grasslands was bordered by a perennial fallow strip, hedge or tree row. Fallow strips wider than 3 m, hedges and tree rows were mapped as semi-natural non-crop habitats. Landscape parameters for landscape circles around organic and conventional fields forming a pair were averaged for each year. Landscape mosaics were formed by crop fields cultivated with cereals (44% of total landscape area), oilseed rape (8%), sugar beet (4%), maize (2%), and by non-crop habitats including intensively managed grassland (13%), semi-natural habitats such as calcareous grasslands and orchard meadows (10%), forests (8%), fallows (5%), settlements (2%) and others (4%). We used Spearman rank correlations to test correlations between landscape parameters. The proportion of non-crop habitats in both years was positively correlated with the Shannon-index of habitat type diversity (using the percentage values of all habitat types; Steffan-Dewenter 2002) (R = 0·9, P < 0·005), the proportion of grassland (R = 0·8, P < 0·01), and the proportion of forest (R = 0·8, P < 0·01), but not with edge density (R = 0·2, P > 0·4).

Statistics

Linear mixed-effects models (Pinheiro & Bates 2000) were used to analyse effects on species richness and number of brood cells of wasps and bees. Edge density, proportion of non-crop habitats, farming system (organic vs. conventional) and habitat type (field centre vs. fallow strip) were considered as fixed factors, study area and year as random factors.

The following error structure was incorporated in the models (number of levels indicated in parentheses): ‘study area’ (12)/‘year’ (2)/‘farming system’ (2)/‘habitat type’ (2). Statistics for the random factors are shown in Appendix S1. We used Wald tests to test for significance of fixed effects and twofold interactions among them. Fixed factors and interactions that did not contribute to the model with P < 0·05 were removed in a backward stepwise procedure from the full model. Response variables were transformed [log10(x + 1)]. In addition, we tested for polynomial effects of the landscape factors by adding the fixed factors (edge density)2 and (proportion of non-crop habitats)2 to the model. None of these factors had additional explanatory power (P > 0·1) suggesting that the relationships between landscape factors and log-transformed insect diversity and abundance were linear. All statistical analyses were performed using R (R Development Core Team 2005).

Results

In total, 11 193 brood cells of eleven wasp species (2567 brood cells) and seven bee species (8644 brood cells) were collected from 92 trap nest sites (184 trap nest tubes). Eight wasp species were predators of herbivorous insects (75·6% of the wasp brood cells; 1941 brood cells of six eumenid species specialized on lepidopterous larvae and two sphecid species specialized on aphids, Table 2). Three wasp species were specialized predators of spiders (24·4% of the wasp brood cells; 626 brood cells of two sphecid species and one pompilid species, Table 2). Bee communities were dominated by the red mason bee O. rufa L. (95·6% of the bee brood cells; 8266 brood cells of O. rufa; 378 brood cells of other bee species). We recorded 12 species of natural enemies in 2334 host brood cells. Two species of natural enemies (Megatoma undata, Trichodes apiarius), which were found in 82 (3·5%) of the brood cells, were predators, all other natural enemies were (klepto-) parasitoids. Because of the dominance of parasitoids, we refer to natural enemies as parasitoids below. Three species of natural enemies attacked wasps, six species attacked bees, and three species were found in both bee and wasp nests. The drosophilid fly Cacoxenus indagator was the dominant parasitoid of O. rufa (in 94% of parasitized brood cells), which was its only host species (Table 2). Other bees were mainly parasitized by Melittobia acasta (76%), herbivore-predating wasps by Ichneumonidae (48%) and M. acasta (33%), and spider-predating wasps by Ichneumonidaes (33%), Chrysis spp. (30%) and M. acasta (28%). The mortality by natural enemies was 21·9 ± 3·2% (mean ± SE) for wasps and 24·2 ± 1·8% (mean ± SE) for bees.

Wasps

The colonization of trap nests in organic and conventional fields and in adjacent fallow strips was related to the surrounding landscape, the farming system (organic vs. conventional) and the habitat type (wheat field centre vs. fallow strip). At the landscape scale, the species richness of total wasps and of herbivore-predating wasps, and the total number of wasp brood cells increased with increasing edge density (landscape configuration) in landscape circles with 500 m radius (Table 3, Fig. 1a,b). The landscape effect was independent of farming system and habitat type. The proportion of non-crop habitats (landscape composition) had no additional explanatory power. Our data show that a doubling of edge density from 350 to 700 m edge per ha resulted in 260% more wasp brood cells in trap nests.

Table 3.   Final linear mixed-effects models describing the effects of edge density and proportion of non-crop habitat (in landscape circles with 500 m radius), farming system (organic vs. conventional), habitat type (field centre vs. fallow strips) and their interactions on species richness and number of brood cells of wasps
 d.f.FP
  1. Non-significant factors and interactions (> 0·1) were removed in a stepwise backward procedure from the full model.

Total species richness of wasps
 Edge density107·40·022
 Farming system228·30·009
 Habitat type4522·6<0·001
Species richness of predators of herbivores
 Edge density107·50·021
 Farming system224·00·059
 Habitat type4512·9<0·001
Species richness of predators of spiders
 Farming system225·10·035
 Habitat type4523·6<0·001
Total brood cell number of wasps
 Edge density105·20·046
 Farming system226·90·016
 Habitat type4419·8<0·001
 Farming system × habitat type444·60·038
Brood cell number of predators of herbivores
 Farming system223·70·068
 Habitat type4410·50·002
 Farming system × habitat type444·60·036
Brood cell number of predators of spiders
 Habitat type4421·8<0·001
Figure 1.

 Effects of the landscape context (edge density and % non-crop fields in 500 m radius) on species richness and brood cell numbers of wasps and bees. Results are based on mixed-effects models (see Table 2). Data of the two study years were averaged for each of the four site types per study area (conventional/organic field centre/fallow strip).

At the local scale, the species richness of wasps and the total number of wasp brood cells were higher in organic than in conventional sites and higher in fallow strips than in field centres (Table 3, Fig. 2a). The species richness of herbivore-predating and spider-predating wasps reflected the results found for the species richness of total wasps (Table 3). An interaction between farming system and habitat type indicated that the farming system influenced the number of wasp brood cells in fields and fallow strips differently (Table 3): The mean number of wasp brood cells was more than 200% higher in organic than in conventional fields, whereas the number of brood cells in fallow strips were not influenced by the farming system of the adjacent field. Organic field centres and fallow strips adjacent to both organic and conventional fields had similar numbers of wasp brood cells. Herbivore-predating wasps showed the same pattern as found for the total species richness and total number of brood cells of wasps (Table 3, Fig. 2b). Spider-predating wasps were influenced by habitat type only, with higher brood cell numbers in fallow strips than in organic or conventional field centres (Table 3, Fig. 2c).

Figure 2.

 Species richness of wasps (a) and bees (d), and brood cell numbers of wasps specialized on herbivores (b), of wasps specialized on spiders (c), of the most abundant bee species Osmia rufa (e) and of other bees (without O. rufa) (f) in conventional (black bars) and organic (white bars) fields and adjacent fallow strips. Data of the two study years were averaged for each of the four site types per study area (conventional/organic field centre/fallow strip). Means and standard errors are shown. Results are based on mixed-effects models (see Table 2) with *P < 0·05, **P < 0·01, ***P < 0·001.

Bees

The species richness of bees and the number of brood cells of total bees, of the red mason bee O. rufa and of other bees were positively related to the proportion of non-crop habitats (landscape composition) in a 500 m radius, but not to edge density (landscape configuration, Table 4, Fig. 1). The landscape effect was independent of farming system and habitat type. A doubling of non-crop habitats from 30% to 60% in a landscape circle with 500 m radius resulted in an increase of total bee brood cells of more than 100%. The species richness of bees was higher in organic than in conventional sites (fallow strips and field centres), and higher in fallow strips than in field centres (Table 4, Fig. 2d). For the most abundant bee species O. rufa, organic farming enhanced the number of brood cells significantly, resulting in 30% more brood cells in organic than in conventional fields and 107% more brood cells in fallow strips adjacent to organic than in fallow strips adjacent to conventional fields (Table 4, Fig. 2e). For other bees, the number of brood cells was marginally higher in fallow strips than in field centres (Table 4, Fig. 2f). The total number of bee brood cells was marginally enhanced by organic farming and in fallow strips (Table 4).

Table 4.   Final linear mixed-effects models describing the effects of edge density and proportion of non-crop habitat (in landscape circles with 500 m radius), farming system (organic vs. conventional), habitat type (field centre vs. fallow strips) and their interactions on species richness and number of brood cells of bees
 d.f.FP
  1. Non-significant factors and interactions (> 0·1) were removed in a stepwise backward procedure from the full model.

Total species richness of bees
 Proportion of non-crop habitats1013·80·004
 Farming system224·70·041
 Habitat type456·60·014
Total brood cell number of bees
 Proportion of non-crop habitats106·90·025
 Farming system224·10·056
 Habitat type453·20·080
Brood cell number of Osmia rufa
 Proportion of non-crop habitats104·50·058
 Farming system225·10·034
Brood cell number of other bees
 Proportion of non-crop habitats107·40·022
 Habitat type453·70·060

Parasitoids

Species richness of parasitoids and number of parasitized brood cells increased with increasing host species richness and increasing number of host brood cells for herbivore-predating wasps and spider-predating wasps (models with two fixed factors; all P < 0·005). For O. rufa and for ‘other bees’ species richness of parasitoids and number of parasitized brood cells increased with increasing number of host brood cells only (all P < 0·004).

Although effects of local and landscape factors on parasitoids were mediated by host abundance and host species richness, patterns of parasitized brood cells slightly differed from what we expected according to host patterns. Parasitoids of the bee O. rufa were more sensitive to habitat quality than their hosts, parasitoids of ‘other bees’ and of herbivore-predating wasps were less sensitive. For O. rufa, the number of parasitized brood cells, but not of total host brood cells was lower in field centres than in fallow strips, resulting in a marginally lower parasitism rate in field centres (Table 5). The number of brood cells of ‘other bees’ and of herbivore-predating wasps, but not the number of parasitized brood cells was lower in field centres and in conventional sites, respectively. These divergences resulted in marginally higher parasitism rate in field centres for ‘other bees’, and in conventional sites for herbivore-predating wasps (Table 5).

Table 5.   Final linear mixed-effects models describing the effects of farming system (organic vs. conventional) and habitat type (field centre vs. fallow strips) on numbers of parasitized brood cells, numbers of host brood cells, and resulting parasitism rates. Landscape factors and interactions did not explain additional variance (> 0·05)
Explanatory variablesResponse variables
Number of parasitized brood cellsNumber of host brood cellsParasitism rate
d.f.FPPd.f.FP
  1. For comparison, P-values of the number of host brood cells are indicated by ***< 0·001, **< 0·01, *< 0·05 and (*)< 0·1, corresponding to the values shown in Tables 3 and 4.

Herbivore-predating wasps
 Farming system  NS(*)163·50·079
 Habitat type456·00·018**  NS
 Effect direction: farming systemNo effectOrg > convOrg < conv
 Effect direction: habitat typeFallow > fieldFallow > fieldNo effect
Spider-predating wasps
 Habitat type4513·2<0·001***  NS
 Effect direction: habitat typeFallow > fieldFallow > fieldNo effect
Osmia rufa
 Farming system225·10·034*  NS
 Habitat type456·40·015NS383·40·071
 Effect direction: farming systemOrg > convOrg > convNo effect
 Effect direction: habitat typeFallow > fieldNo effectFallow > field
Other bees
 Habitat type  NS(*)47·30·054
 Effect direction: habitat typeNo effectFallow > fieldFallow < field

Discussion

The results of our study support our hypotheses that factors at all spatial scales, including farming system, habitat type, landscape composition and connectivity, contribute to the explanation of nest colonization patterns. Cavity-nesting bees and wasps depend on nesting sites in non-crop habitats, but forage in multiple habitats including crop fields in a complex and little known way. The relative importance of landscape composition vs. configuration and of habitat type vs. farming system depended on the species group tested. Differences between parasitoids and their hosts resulted in changes in parasitism rates.

Bees were enhanced by high proportions of non-crop habitat (landscape composition), whereas wasps were enhanced by high edge densities (landscape configuration). Edge density is positively related to the length of linear non-crop features such as bank vegetation, fallow strips, hedges and tree rows which lie parallel to the field edges. The positive effect of edge density rather than of total area of non-crop habitat for nest colonization by wasps suggests that field edges provided connectivity and facilitated wasp movements between trap nests and source habitats where dispersal started (Fried, Levey & Hogsette 2005). This supports experimental findings showing benefits of grass strip corridors for nest colonization by wasps (Holzschuh et al. 2009). In contrast, bee colonization may have been enhanced by a high number of source populations, when the amount of non-crop habitat in the landscapes is high, independent of connectivity. The differing response of bees and wasps to landscape factors may have consequences for pollination and predator–prey systems: while bees may provide pollination services within at least 500 m radius around their non-crop nesting habitats, predation by wasps may decline and predator–prey interactions may shift in favour of prey in landscapes where boundary structures are missing.

Landscape configuration and composition affected trap-nesting wasps and bees in both habitat types and both farming systems similarly. In studies on flower-visiting bees landscape and local factors were found to interact with each other: diversity decreased with decreasing landscape heterogeneity in conventional fields, but not in organic fields, indicating that organic fields compensated for lacking non-crop foraging habitats in homogeneous landscapes (Holzschuh et al. 2007; Rundlöf et al. 2008). In contrast to the majority of flower-visiting bees, which are mainly ground-nesting, trap-nesting bees seem to be limited by a lack of nesting resources (affecting bees in both organic and conventional fields) rather than by a lack of flower resources at the landscape scale (affecting bees in conventional fields more strongly). We conclude from our study that for cavity-nesting bees and wasps organic fields cannot compensate for missing nesting resources in non-crop habitats at the landscape scale.

While landscape characteristics determine where dispersing individuals can come from, local factors may affect their final colonization decision. We hypothesized that nest colonization is higher in fallow strips than in field centres, and higher under organic than under conventional farming methods. Both organic farming and fallow strips enhanced the diversity and abundance of wasps and bees compared to conventional farming and wheat field centres. A meta-analysis revealed that there are great beneficial effects of organic farming on plants and predatory insects, while effects on non-predatory insects and pests are small (Bengtsson et al. 2005). While bees may benefit from the absence of agrochemicals and a higher abundance and diversity of flowering plants in organic fields (Holzschuh et al. 2007), predatory wasps may prefer organic fields due to a higher abundance of spiders, aphids and lepidopteran larvae, which are used for nest provision (Tscharntke et al. 1998; Schmidt et al. 2005). Our results show that even non-crop nesting specialists do not generally perceive cereal fields as hostile landscape matrix. The positive effect of organic compared to conventional farming underlines the impact of local food availability on nest colonization (Tscharntke et al. 1998) and revealed the potential importance of cereal fields in providing those food resources.

Interestingly, the positive effect of organic field management also influenced adjacent fallow strips which did not differ in their management. Positive effects of organic farming on adjacent habitats have been recorded in plants (Aude et al. 2004) and from pollinators (Feber et al. 2007; Holzschuh, Steffan-Dewenter & Tscharntke 2008). They may result from the absence of agrochemical drift from fields into adjacent habitats (Marshall & Moonen 2002) and/or – in the case of pollinators – from the benefits provided by the flower resources in organic fields. For the bee O. rufa, positive effects of organic farming on abundances in adjacent fallow strips were even stronger than positive effects of fallow strips vs. field centres. This was in contrast to our expectation that fallow strips are generally better bee habitats than cereal fields, because they provide higher plant diversity and might be perceived as less hostile than crop fields, which never provide nesting sites (Fussell & Corbet 1991; Bäckmann & Tiainen 2002; Pywell et al. 2005, 2006; Feber et al. 2007). Our results indicate that a habitat type that is generally considered to be valuable for bees does not necessarily enhance bee abundance. Low (food-resource) quality of the adjacent crop habitat can reduce the quality of the non-crop habitat enormously.

Based on a previous study showing that eumenid wasps prefer flying along fallow strips instead of crossing conventionally managed cereal fields (Holzschuh et al. 2009) and our results on landscape scale effects (see above), we expected great differences between trap nests in field centres and fallow strips for herbivore-predating wasps. Our data on local effects confirm this expectation for conventional fields, but not for organic fields. Organic farming increased the value of wheat fields for predators of herbivores to the level of fallow strips. This is remarkable, because fields were more homogeneous than fallow strips, even despite the higher weed diversity in organic fields. Apparently, the hostility of conventional wheat fields does not result from the structure of a cereal monoculture per se, but rather from the lower food availability compared to organic fields.

Food availability may influence the abundances in trap nests in two ways: reproduction may be enhanced, if high food availability reduces the time spent on collecting food for larval provision; colonization is enhanced, if colonizing females prefer nests in the vicinity of flowering plants or abundant prey (Klein, Steffan-Dewenter & Tscharntke 2004, 2006; Albrecht et al. 2007). A high number of brood cells can be explained either by a high number of females that colonized the trap nest or by a high reproduction per colonizing female. In contrast, high species diversity can only be explained by a high number of females that colonized the trap nests, but not by high reproduction rates per female. Thus, adults presumably, prefer nests in the vicinity of abundant food resources, so high numbers of brood cells may be mainly explained by a preference for those nesting sites.

Finally, we tested the hypothesis that parasitoids are more affected by agricultural intensification than their hosts. Parasitoid species richness and abundance were well-explained by both host species richness and host abundance suggesting that parasitoids were most abundant and diverse in heterogeneous landscapes, organic sites and fallow strips. However, parasitoids of herbivore-predating wasps and bees other than O. rufa were less sensitive to agricultural intensification and reduced habitat quality than their hosts resulting in marginally higher parasitism rates in conventional sites and field centres respectively. Only parasitoids of the bee O. rufa were found to be more sensitive than their hosts resulting in marginally lower parasitism rates in field centres than in fallow strips. Parasitism rates of trap-nesting bees and wasps decreased with increasing distance from extensively managed grasslands in Germany and Switzerland (Tscharntke et al. 1998; Albrecht et al. 2007) and from forest edges in Indonesia (Klein et al. 2006) suggesting that parasitoids were disadvantaged when following their hosts into more disturbed habitats. In contrast, parasitism rates in trap nests did not decrease in smaller and more isolated orchard meadows in central Europe (Steffan-Dewenter & Schiele 2008) and even increased with increasing habitat modification from rain forest to rice paddies in Ecuador (Tylianakis, Tscharntke & Lewis 2007) showing that generalist parasitoids did not suffer as strongly from agricultural intensification as their hosts. Based on theoretical considerations, specialists, not generalists, of higher trophic levels are expected to be more affected by disturbances than their hosts, suffering from smaller population sizes and patchy distributions (Holt et al. 1999; Tscharntke et al. 2005). Local population dynamics of host species make them an unstable resource for species of higher trophic levels. Theory predicts that specialist parasitoids depend on recolonization processes more strongly than their hosts (Kruess & Tscharntke 1994). Our results underline that changes in land use intensity and habitat quality can result in changed trophic interactions, but the direction of changes are not generally predictable. Host species which are dominantly parasitized by rather specialized species such as the drosophilid fly C. indagator (host: O. rufa) may be able to escape from parasitism by colonizing more disturbed habitats. In contrast, species parasitized by generalist species like the parasitic wasp M. acasta appeared to suffer twice from agricultural intensification: from direct negative effects and additionally from increased parasitism rates in more disturbed habitats.

Habitat loss, habitat fragmentation and reduced habitat quality contributed to the reduction of diversity and abundance of cavity-nesting bees, wasps and parasitoids in agricultural landscapes. However, differences in the perception of landscape and local factors among species groups indicate that effects of agricultural intensification, which take place at several scales simultaneously, are not easily predictable. Non-crop nesting specialists do not necessarily perceive crop fields as a hostile landscape matrix – at least if fields are less intensively managed, and do not necessarily favour fallow strips, because high management intensity in the adjacent crop field can reduce their quality. Perennial fallow strips and other edge habitats are not only important for local recolonization processes from field edges into field centres (Landis, Wratten & Gurr 2000), but facilitated even nest colonization by wasps at the landscape scale. Interestingly, habitat connectivity appeared to be enhanced by both higher edge densities (higher perimeter-area ratios) and higher percentage of organic farming. Conversion of crop land into non-crop habitat may not be a sufficiently successful strategy to enhance wasps or other species that suffer more from isolation than loss of habitat. Consequently, related ecosystem services such as pollination and biological control by bees and wasps are threatened by habitat loss and land use intensification at different spatial scales.

Acknowledgments

We thank the farmers for their participation in the project, Yann Clough for help with the site selection and for statistical advice, Doreen Gabriel for GIS-support, Gundula Kolb for help with the dissection of trap nests, Reiner Theunert for help with species identification and Rachel Gibson, Emily Martin, Ken Norris and two anonymous reviewers for their helpful comments. This research was carried out within the framework of the EU-funded project ‘EASY’ (QLK5-CT-2002-01495) coordinated by David Kleijn and the BESS (Biotic Ecosystem Services) project of Carsten Dormann.

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