Wild Bees Respond Complementarily to ‘High-Quality’ Perennial and Annual Habitats of Organic Farms in a Complex Landscape

Journal of Insect Conservation (2018) 22:551–562 https://doi.org/10.1007/s10841-018-0084-6

ORIGINAL PAPER

Wild bees respond complementarily to ‘high-quality’ perennial and annual habitats of organic farms in a complex landscape

Lukas Pfiffner1 · Miriam Ostermaier1,2 · Sibylle Stoeckli1 · Andreas Müller3

Received: 10 January 2018 / Accepted: 18 August 2018 / Published online: 21 August 2018 © Springer Nature Switzerland AG 2018

Abstract Agricultural intensification leads to large-scale loss of habitats offering food and nesting sites for bees. This has resulted in a severe decline of wild bee diversity and abundance during the past decades. There is an urgent need for cost-effective conservation measures to mitigate this decline. We analysed the impact of five different high-quality habitats on species richness and abundance of wild bees in a complex landscape of north-western Switzerland at six sites. The five habitat types included 45 plots situated on eight organic farms and were composed of 16 low-input meadows, six low-input pastures, seven herbaceous strips adjacent to hedges, five sown flower strips and eleven organic cereal fields. All of them are financially subsidised by the Swiss agri-environmental scheme. Wild bees were sampled between the end of April and end of August 2014 by using trio-pan traps and complementary sweep netting on these five habitat types. On 45 plots we recorded 3973 bee specimens, belonging to 91 species, 16 of which are red listed, revealing a high bee species richness in the study area. Wild bee species richness and abundance were best explained by habitat type, number of flowering plants and site. A strong relationship of increasing number of flowering plants and bee species richness and abundance was found. Grassland habitats, especially low-input meadows, harboured the highest species richness and abundances. Organic cereal fields showed a potential to conserve bee species relevant to nature conservation (harbouring exclusively two red list species and four rare species). Ordination analysis of the bee communities showed a relative dissimilarity between the habitat types and indicates their complementary effects to benefit the diversity of wild bees. Our results demonstrate that a matrix of low-input habitats are needed to sustain rich assemblages of wild bees in agroecosystems.

Keywords Wild bees · Agri-environmental scheme · Biodiversity · Semi-natural habitats · Low-input habitats · Sustainable agriculture

Introduction

Wild bees and other pollinators play a crucial role in the reproduction of wild and crop plants (Kleijn et al. 2007). Bees belong to the most important pollinators worldwide, and their ongoing severe decline in many agricultural land- Electronic supplementary material The online version of this scapes during the past decades and its potential economic article (https://doi.org/10.1007/s10841-018-0084-6) contains and ecological consequences are therefore of major concern supplementary material, which is available to authorized users. (Biesmeijer et al. 2006; Potts et al. 2010). Of the 109 most * Lukas Pfiffner important crop plants, 87 species are entirely dependent on [email protected] pollination by insects (Kleijn et al. 2007; Sardinas and; Kre- men 2015). The loss of these pollinators is likely to lead 1 Research Institute of Organic Agriculture (FiBL), to negative impacts on both general biodiversity and crop Ackerstrasse 113 / P.O. 219, 5070 Frick, Switzerland productivity (Burkle et al. 2013). 2 Restoration Ecology, Technical University Munich, Anthropogenic land use change and agricultural inten- Emil‑Ramann‑Str. 6, 85350 Freising, Germany sification are considered to be among the main drivers 3 Natur Umwelt Wissen GmbH, Universitätstrasse 65, of the decline in bee diversity. Decline in pollinators has 8006 Zurich, Switzerland

Vol.:(0123456789)1 3 552 Journal of Insect Conservation (2018) 22:551–562 been attributed to removal and deterioration of semi-nat- Our study aimed to investigate how populations of ural habitats and other interstitial non-crop habitats rich wild bees are affected by habitat type and habitat quality in pollen and nectar (Biesmeijer et al. 2006; Roulston within a complex structured landscape. Therefore we have and Goodell 2011) and intensive farming on crop land. selected semi-natural habitats subsidised by the Swiss agri- Intensive farm practices negatively impact wild bees in environmental scheme (Swiss Confederation 2013). These different vital aspects of food and nesting resources: (i) habitats show a great potential to provide flower and nest- high input of fertilisers and herbicides and intensive land ing resources for wildbees. They are extensively managed, use of grassland reduces floral diversity in fields and field unfertilised and are finally assumed to provide an abun- margins (Power and Stout 2011; Clough et al. 2007); (ii) dance of pollen and nectar for many bee species: there were insecticides and other pesticides that cause direct mortal- flower-rich, high-quality habitats as low-input meadows, ity or sub-lethal effects (Gill et al. 2012; Whitehorn et al. extensively used cattle pastures, sown flower strips and her- 2012; Goulson et al. 2015); (iii) high disturbances by till- baceous strips adjacent to hedges. Furthermore, we included age and harvesting techniques, impeding nesting of most organic cereal fields to assess the potential of a low-input ground nesting species (Winfree et al. 2009; Clough et al. annual crop for the promotion of bee diversity. 2014) and (iv) the loss of uncut vegetation, uncropped field margins and microstructures as dead wood, stone pil- lows (Winfree et al. 2009). Materials and methods Agri-environmental schemes in European countries pri- oritise on-farm habitat creation providing incentives through Study area cost-share programs (Aviron et al. 2009). Despite these programs, there is little evidence about the effectiveness of The study region was situated in the lowland of the Northern these semi-natural habitats and field margins (Pe’er et al. part of Switzerland (Canton of Aargau). It is a hilly region in 2014), and specifically, whether they can sustain pollinator the Frick valley, with a rural, diverse landscape characterised services (Garibaldi et al. 2011; Kovács-Hostyánszki et al. by agricultural and forest land use and some small villages. 2017). The climate is characterised by an average temperature of Flower diversity significantly affects species diversity of 9 °C, a mean sunshine duration of 1620 h per year and a wild bees, since almost half of the central European species mean precipitation of 1081 mm per year. The agriculture is collect pollen exclusively from a single plant genus or fam- generally semi-intensive with a diversity of grassland, arable ily. No less than 28 different plant genera and 20 different and horticulture crops. plant families serve as these specialized species that provide We analysed five different habitat types for species rich- exclusive sources of pollen (Zurbuchen and Müller 2012). ness and abundance of wildbees, and selected 45 plots at Flower abundance significantly affects reproductive success six sites in a complex landscape (see Table S1, in Support- as the wild bees’ quantitative pollen requirements for feeding ing Information). We have selected all possible high-quality their larvae are very high. The wild bee Megachile parietina, habitats on eight highly consolidated organic farms, if neces- for example, needs pollen from 1140 flowers of Common sary we have used habitats of two farms to get a sufficient Sainfoin (Onobrychis viciifolia) to provision one single number of 6–10 plots per site. This was the case at sites offspring (Müller et al. 2006). Most wild bees have short in Wegenstetten and Möhlin.The plots were at least 500 m periods of flight activity, lasting only a few weeks with dif- apart to minimize interaction. The landscape is characterised ferent species flying in spring, early summer and late sum- by one-fifth or more grassland, mostly < 20% arable land, mer respectively. Therefore the provision of a succession of often surrounded by forest (up to 43%), and with 3–14% floral resources from early spring to late summer is essential semi-natural habitats and 15% settlements with garden (cal- to maintain species diversity in a given landscape (Oertli culated within the radius of 800 m, Table S2). All eight et al. 2005). A continuous supply of flower resources is also farms were certified as organic farms by the Bio Suisse crucial for social bees, such as bumblebees, which need large farming association (Swiss Confederation 2010). Sixteen pollen and nectar quantities from early spring to late sum- low-input meadows, six low-input cattle pastures, seven mer to allow colony development. Considering endangered herbaceous strips along hedgerows, five sown flower strips and specialized species, there is a knowledge gap referring with native plants and eleven organically cultivated cereal to the question of how far these species can be enhanced by fields were investigated. These areas were selected as they different flower-rich, extensively managed habitats in a com- were all enrolled in agri-environmental schemes of Switzer- plex landscape dominated by agricultural land-use. However land, for which farmers are subsidised (Swiss confederation these semi-natural habitats play a key role in the retention 2013). They were characterized by low-input farming and of functionally diverse bee assemblages in agroecosystems as unfertilized habitats excluding cereal fields. Cereal fields (Forrest et al. 2015; Garibaldi et al. 2014). were chosen as a reference for a low-input annual crop to

1 3 Journal of Insect Conservation (2018) 22:551–562 553 make a comparison with perennial semi-natural habitats. mainly represented by small villages with numerous house The low-input meadows were either mown once or twice gardens. The percentage of land use types was calculated per year, with most of them contained nesting microstruc- with QGIS 2.6.0. tures, such as dead wood and piles of stones and also an uncut strip as temporary foraging area (Table 1). Herbaceous Bee sampling strips were natural grown elements adjacent to a hedge, and flower strips are sown, species-rich elements with native Bees were sampled using trio-pan traps, complemented by plants. Two-thirds of flower strips were adjacent grassland sweep netting along variable transects (Sutherland 2006). and one-third surrounded by arable fields. The size of the Pan traps are known as a powerful standardised method to sampling area differed depending on the habitat type. Mean examine wild bees (Westphal et al. 2008). A trio-pan trap area of flower strips was 0.29 ha, herbaceous strips 0.12 ha, consisted of one white, one yellow and one blue plastic bowl low-input meadows 0.48 ha, low-input pastures 0.61 ha and with a diameter of 14.8 cm. Pan traps were filled with 300 ml cereal fields 1.82 ha (see details in Table 1). of water and some detergent. Pan traps were placed at the current vegetation height and adjusted to the changing veg- Habitat characterisation etation height during the study period. Each exposure time of the pan traps was standardised through the sunshine dura- All study plots were characterised by the number of flow- tion, determined by the nearest monitoring station of the ering plant species, flower cover, bare soil cover and nest- Federal office of Meteorology and Climatology MeteoSwiss. ing microstructures. The number of flowering plants and The pan traps were collected after 27–37 h sunshine, after the percentage of dicot flower cover were recorded in three about 3–10 days depending on hours of sunshine every day. 1 m2-plots per plot in each sampling period. The percentage Bees were sampled from 22th April to 29th August 2014. of bare soil was recorded in each sampling period as a proxy The survey was performed during five time-periods, once of nesting sites for ground-nesting guilds (Sardinas and Kre- a month, to take into account the seasonality of wild bees men 2014). Dead wood, dead plant stems and piles of stones and thus to obtain a representative overview of the wild bee as important nesting microstructures were recorded once species in the selected habitats (Sutherland 2006). The trio- during the study period. The surrounding landscape was pans and sweep-netting were located at least 30 m from the characterized in a radius of 800 m around the study plots, border of the study plots to reduce edge effects (excluding assuming that the flight distance of most wild bee species is the strips due to their narrow width). We applied variable within this range in a complex landscape (Zurbuchen et al. transect sampling as complementary method (Sutherland 2010). Land use was categorised into arable land, grass- 2006). This means that an area of 240 m2 within the study land, ecological compensation area, forest and settlement. plots showing rich flower cover was chosen for sweep net- Grasslands were mainly high-input meadows which regu- ting. During 15 min the chosen area was walked through larly fertilized and were four to five times cut per year. The and wild bees were netted, optimising the sampling of the category ecological compensation areas include low-input present bee species (Westphal et al. 2008). Sweep netting meadows, low-input pastures, hedges, sown flower strips, was always conducted under sunny weather conditions which were part of the Swiss agri-environmental program when bees were most active (temperature over 15 °C, cloud and considered as semi-natural habitats. Settlements were cover < 30%, between 10.00 and 17.00 h). All bees were

Table 1 Characterization of habitat types: farm practices management and offered options of food and nesting resources Management Habitat type Mean area (ha) Fertilizer Cutting, harvest regime Remarks

Low-input meadows 0.48 ± 0.33 Unfertilized 1–2, 1st cut mostly around mid of June, leaving an Rich in plant speciesa uncut refugee Low-input pasture 0.61 ± 0.25 Unfertilized 1—always grazed, mostly after 24.5 Cow pasturesa Herbaceous strips 0.12 ± 0.07 Unfertilized 0–2, 1st cut mostly around mid of June, leaving an Adjacent to hedges a uncut refuge (about 50%) Flower strip 0.29 ± 0.16 Unfertilized 0–2, 1st cut mostly around mid of June, leaving a Sown native plants, rich in plant spec. uncut refuge (about 10%) Organic cereal fields 1.82 ± 1.37 Slurry or After harvest-period from mid/end of July Winter cereals (73% winterwheat) compost manure a Piles of stones and branches as nesting microstructures

1 3 554 Journal of Insect Conservation (2018) 22:551–562 identified to species level in the lab, whereas domesticated each other and tested for significant correlation to iden- honeybees (Apis mellifera) were excluded from all analyses. tify possible collinearity (especially between number of The nomenclature follows the catalogue of the bees of Swit- flowering plants and flower cover). Models were carried zerland, Austria and Germany (Schwarz et al. 1996). out separately using each correlated factor. The model selection was continued only with one of two correlated Data analyses factors based on the AIC. The post hoc general linear hypothesis test (GLHT) with Tukey contrast using the The total number of species and abundances from trap and R package multcomp (Hothorn et al. 2015) was used for net sampling were analysed as pooled data, as the sampling post hoc analyses. Species abundance was transformed methods are known to be complementary (Westphal et al. using log(x + 0.5) to meet the assumption of normality 2008). Total pooled wild bee species richness and abun- (Sokal and Rohlf 1995). The percentage of flower cover dance per plot (including rare species) during the sampling and bare soil were transformed using an arcsine transfor- period were determined as dependent variables. In addition mation (arcsine of the square root of the proportion). All to the total pooled data, bumblebees, endangered and oli- explanatory covariates were scaled to one standard devia- golectic bee species were analysed separately. Bumblebees tion. Bayesian methods were used (Zuur et al. 2009). The were distinguished from other wild bees because these two sim function of the arm package in R was used to draw groups have different biological traits in terms of floral random 10,000 simulations from the joint posterior dis- requirements, flying abilities and sociality (Gathmann and tribution of the parameters from the final model (Gelman Tscharntke 2002; Michener 2007) so that different responses and Su 2014). Based on the quantiles of these simulated to agricultural land use and habitats are expected. Due to samples from the posterior distributions, the 95% credible high relevance for nature conservation, endangered (Amiet interval (CrI) was obtained for each model parameter. If 1994) and/or oligolectic bees (Westrich 1990) were analysed zero was not included in the 95% CrI, a significant effect separately. As explanatory variables habitat type, number was denoted. The effect of habitat type on the number of of flowering plant species, flower cover, and bare soil cover flowering plant species, flower cover and bare soil cover were considered. The mean value per season for flower cover were analysed using a linear model with an identity link and soil cover was used, whilst the number of flowering function (LM). The difference between habitat types was plant species was summed for each time period and across analysed using multiple comparisons, with the post hoc all periods for statistical analysis. “GLHT” with Tukey contrast. To analyse the spatio-tem- All statistical analyses were carried out with R 3.1.2 (R poral complementarity of the different habitats, a model Development Core Team 2014; Giraudoux 2014). Species including habitat type as fixed factors and site as well as richness was analysed with a generalized linear model with plot as a random term was carried out separately for each Poisson errors and a log link function, and abundance with a time-period (I–V). linear model with an identity link function (Zuur et al. 2009; Finally, we compared the bee communities between dif- Bates et al. 2014) (Table 2). Habitat, number of flowering ferent habitats using non-metric multidimensional scaling plant species, flower cover, bare soil cover and site were (NMDS). NMDS is an ordination method and substitutes included as fixed factors. Two and three way interactions the original distance between the objects with ranks. The between habitat, flowering plant species, flowering cover and meta function NMDS from the R vegan package considers bare soil cover were included in the full model. We tested the Bray–Curtis dissimilarity index and several random if all model assumptions were met (residual analyses). The starts to perform NMDS. Data were square root trans- spatial autocorrelation was estimated by the function acf formed to meet monotony and the number of dimensions of the R package stats (R Development Core Team 2014). was assessed, estimating the variability of the stress for Overdispersion was checked looking at the ratio of residual 2–7 dimensions in a Shepard diagram. The stress value deviance to degrees of freedom. There was no significant indicates the goodness of fit of the NMDS ordination com- overdispersion and temporal autocorrelation. The number pared to the original calculated distance matrix, with a of species and individuals of wild bees, as well the number stress value of 0.1–0.5 representing an excellent ordination of flowering plant species, flower cover and bare soil cover and 0.5–1 still showing a good ordination (Borcard et al. in different habitats was analysed using (generalised) lin- 2011). The stress factor for K = 2 dimensions was 0.27 ear mixed models with site as random term (Fig. 1). When and therefore two dimensions provided a sufficient ordina- looking just at one specific explanatory variable, site was tion. In addition the goodness-of-fit of the ordination was included as random term to prevent spatial autocorrelation. analysed using non-linear regression (R 2) of the NMDS A step-wise backward model selection, using Akaike distances on the original distances. For K = 2 dimensions information criterion, was carried out (AIC; Zuur et al. with R2 = 0.92. 2009). Each explanatory variable was plotted against

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Table 2 Impact of different explanatory variables on wild bee species richness and abundance Wild bees Richness Abundance Model AIC 264.96 45.7 Median CrI 95% CrI (2.5%; 97.5%) Median CrI 95% CrI (2.5%; 97.5%)

Intercept 2.95 2.75, 3.14 4.33 4.01, 4.64 Habitat-type LIP − 0.22 − 0.47, − 0.02 − 0.24 − 0.65, 0.15 HeSt 0.04 − 0.23, 0.32 − 0.06 − 0.49, 0.38 FlSt − 0.35 − 0.62, − 0.08 − 0.46 − 0.87, − 0.05 OCF (Getr) − 0.17 − 0.52, 0.17 0.06 − 0.49, 0.60 No of flowering plants 0.12 0.02, 0.27 0.36 0.12, 0.59 Site Hellikon − 0.02 − 0.28, 0.23 − 0.20 − 0.61, 0.21 Moehlin − 0.03 − 0.25, 0.19 − 0.14 − 0.50, 0.20 Olsberg 0.29 0.03, 0.56 0.61 0.17, 1.03 Wegenstetten − 0.06 − 0.37, 0.22 − 0.65 − 1.13, − 0.17 Woelflinswil − 0.01 − 0.27, 0.27 0.61 0.17, 1.03 Bumblebees Richness Abundance Model AIC 180.50 85.96 Median CrI 95% CrI (2.5%; 97.5%) Median CrI 95% CrI (2.5%; 97.5%)

Intercept 1.81 1.45, 2.17 2.49 1.91, 3.06 Habitat-type LIP − 0.82 − 1.50, − 0.12 − 0.74 − 1.35, − 0.12 HeSt − 1.02 − 1.76, − 0.26 − 1.04 − 1.80, − 0.27 FlSt − 1.84 − 3.42, − 0.28 − 0.14 − 0.77, 0.49 OCF − 1.90 − 4.12, 0.34 − 1.38 − 2.51, − 0.22 Flower cover − 0.23 − 0.63, 0.17 − 0.10 − 0.56, 0.36 Interaction Habitat-type × Flower Cover LIP × Flower cover 0.56 − 0.54, 1.67 – – HeSt × Flower cover − 0.16 − 1.32, 1.00 – – FlSt × Flower cover 1.69 0.20, 3.18 – – OCF × Flower cover − 0.37 − 1.92, 1.17 – – Site Hellikon – – − 0.39 − 1.04, 0.26 Moehlin – – − 0.54 − 1.09, − 0.01 Olsberg – – 0.13 − 0.54, 0.822 Wegenstetten – – 0.18 − 0.47, 0.84 Woelflinswil – – − 0.52 − 1.18, 0.13 Oligolectic bees Richness Abundance Model AIC 148.56 124.53 Median CrI 95% CrI (2.5%; 97.5%) Median CrI 95% CrI (2.5%; 97.5%)

Intercept 0.22 − 0.37, 0.79 0.52 0.24, 0.80 Habitat-type LIP 0.16 − 0.55, 0.88 – – HeSt 0.41 − 0.50, 1.29 – – FlSt − 0.96 − 2.00, − 0.03 – – OCF 0.27 − 1.10, 1.71 – – Flower cover 0.60 0.08, 1.12 0.38 0.09, 0.66

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Table 2 (continued) Red List bees Richness Abundance Model AIC 159.62 125.23 Median CrI 95% CrI (2.5%; 97.5%) Median CrI 95% CrI (2.5%; 97.5%)

Intercept 0.97 0.45, 1.48 2.65 1.88, 3.38 Habitat-type LIP − 0.03 − 0.74, 0.66 − 0.26 − 1.22, 0.68 HeSt 0.40 − 0.29, 1.11 0.25 − 0.81, 1.32 FlSt − 0.38 − 1.11, 0.35 − 0.94 − 1.92, − 0.04 OCF − 0.22 − 1.16, 0.73 − 0.04 − 1.37, 1.26 No of flowering plants 0.19 − 0.21, 0.59 0.49 − 0.07, 1.07 Hellikon − 0.77 − 1.64, − 0.07 − 1.82 − 2.81, − 0.82 Moehlin − 0.08 − 0.65, 0.50 − 0.69 − 1.55, 0.17 Olsberg 0.52 − 0.16, 1.22 − 0.26 − 1.29, 0.76 Wegenstetten − 0.87 − 1.80, − 0.06 − 2.49 − 3.62, − 1.30 Woelflinswil 0.03 − 0.70, 0.74 − 0.03 − 1.07, 1.01

The final generalized linear model (GLM; richness) and the linear model (LM; abundance) was selected based on the Akaike information criterion (AIC). We present the median and the 95% credible interval (CrI) (i.e. from 2.5 to 97.5%) of the posterior distribution of the GLM and LM. The median is in bold if zero is not included within the 95% CrI (effect significantly different from zero) LIM low-input meadows, LIP low-input pasture, HeSt herbaceous strips, FlSt flower strip, OCF organic cereal fields

Fig. 1 Number of species (a) and individuals (b) of wild bees in dif- linear mixed models (number: GLMM; abundance: LMM). The different habitats: low-input meadows (LIM), low-input pasture (LIP), ference between habitat types was analysed using multiple compari- herbaceous strips adjacent to hedgerows (HeSt), flower strip (FlSt), sons, with the post hoc “general linear hypothesis test” (GLHT). Dif- and organic cereal fields (OCF), with mean ± SEM. The relationship ferent letters shows significant differences between habitat types and wild bees was tested using (generalised)

Results Variables influencing bee species richness and abundance We recorded 91 species and 3973 specimens of wild bees in the 45 study plots, which included five habitat types Using a full model based on AIC criterion showed that bee (Table S3). 16 of the recorded bee species were bumble- species richness and abundance was best explained by habi- bees, 19 were oligolectic and 16 were endangered species tat type, number of flowering plants and site (Table 2). Bare of the red list. Surprisingly, 31 species (= 34% of all spe- soil cover and interactions were not significant parameters in cies) were exclusively recorded in one habitat type, mostly the final model for species richness and abundance. A strong as singletons or doublets; seven of them are red listed, relationship of increasing number of flowering plants and eight are oligolectic and three belong to the bumblebees bee species richness and abundance was found (Fig. 2a, b). (Table S3). Bumblebee richness and abundance were significantly related to habitat type (Table 2). There was an interaction

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30 (a) 300 (b)

250 25

200

20 150

Species richness 100

15 Species abundance

10 0

51015202530 51015202530 No of flowering plants No of flowering plants

Fig. 2 Relationship between No. of flowering plants and wild bee speciesa richness or b abundance. Shown are regression lines including 95% credible intervals (Cr). Red line: median CrI. Blue dotted line: 2.5% and 97.5 CrI. The factors were fixed as LIM (Habitat-type) and Frick (Site) between habitat type and flower cover on bumblebee rich- organic cereal fields and herbaceous strips (Fig. 1b). There ness. Therefore a positive relationship between flower cover were no significant differences between low-input meadows and bumblebee richness was identified for low-input pastures and low-input pastures. (not significant) and flower strip (significant), but not for the The richness and abundance of bumblebee and oligolectic other habitats. Furthermore, the site had a significant effect bees were highest on low-input meadows and lowest on on bumblebee abundance. organic cereals fields (Table 3). The number of bumblebee The habitat type and the flower cover had a significant species was significantly higher on low-input meadows com- effect on the richness of oligolectic bee species with higher pared to herbaceous strips and organic cereals fields. The flower cover increasing the number of oligolectic bee species abundance of bumblebee species was significantly higher on (Table 2). The abundance of oligolectic bee species was only low-input meadows compared to low-input pastures, herba- significantly positively related to the flower cover. There was ceous strips and organic cereals fields. Organic cereal fields a significant effect of site on red list bee richness and abun- harboured significantly lower bumblebee individuals com- dance. Finally, we found no significant effect of the habitat pared to flower strips and low-input meadows. The number type on red list species richness and abundance. The number of oligolectic species was significantly higher on low-input of flowering plants had a positive, but not significant effect meadows compared to flower strips and organic cereals on the richness and abundance of red list species (Table 2). fields. Habitat type had no significant effect on oligolectic bee species abundance (Table 3). The highest numbers of Effect of habitat type on the richness red listed species was found in herbaceous strips (richness) and abundance and low-input meadows (abundance), however, richness and abundance in this habitat did not differ significantly com- There was a significant effect of habitat type on the species pared to the other types (Table 3). richness and abundance of wild bees (Fig. 1). The high- The effect of habitat type on wild bee species richness est species numbers were identified on low-input meadows and abundance was additionally analysed separately for and herbaceous strips differing significantly from species each time-period I–V (Figs. S5 and S6). In general, species diversity on cereal fields, which contained the lowest num- richness and abundance increased in all habitat types from ber of species (Fig. 1a). There were no significant differ- time-period I to time-period IV. Our analysis indicates that ences between low-input meadows and herbaceous strips, or the effect of habitat type on wild bee species richness and between flower strips, low-input pastures and organic cereal abundance was more pronounced during time-period I (end fields. The highest abundance was found on low-input mead- of April/May) and II (end of May/June) compared to the ows, differing significantly from abundance on flower strips, other time-periods. At time-period I, species richness and

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Table 3 The species richness and abundance of bumblebee species, oligolectic species, and red-list species found in the different habitats using GLMM Bumblebee species Oligolectic species Red-list species Species richness Abundance Species richness Abundance Species richness Abundance

Low-input meadows 5.2 ± 0.5a 10.0 ± 1.5a 2.1 ± 0.3a 2.9 ± 0.5ns 2.6 ± 0.3ns 16.1 ± 6.7ns Low-input pasture 3.0 ± 0.5ab 5.5 ± 1.3bc 1.8 ± 0.9ab 2.3 ± 1.1ns 2.3 ± 0.8ns 11.9 ± 4.9ns Herbaceous strips 2.6 ± 0.6b 3.9 ± 0.9bc 1.6 ± 0.6ab 2.6 ± 1.0ns 3.1 ± 0.6ns 8.4 ± 2.3ns Flower strip 3.8 ± 1.0ab 7.8 ± 1.7ab 0.8 ± 0.4b 1.2 ± 0.5ns 2.2 ± 0.8ns 4.8 ± 3.1ns Organic cereal fields 2.2 ± 0.3b 2.6 ± 0.4c 0.7 ± 0.3b 0.7 ± 0.3ns 1.7 ± 0.3ns 7.3 ± 3.9ns

The difference between habitat type was analysed using multiple comparisons, with the post hoc “GLHT”. Different letters show significant differences abundance was significantly lower on organic cereal fields highest percent bare soil, followed by low-input meadows, compared to the other habitat types. There was no significant both differing significantly from the percent bare soil in her- difference between the other habitat types. At time-period baceous strips and flower strips (Tukey-HSD, p < 0.05). II, we identified significantly less species numbers and individuals on organic cereal fields compared to herbaceous Dissimilarities of the communities strips adjacent to hedgerows and low-input meadows, but there was no significant difference between the other habitat The NMDS-ordination analysis shows dissimilarities and types. To conclude, our results underline that especially at similarities of the bee communities found on the five differ- the beginning of the season, high quality habitats such as ent habitat types (Fig. 3). The overlapping polygons of the flowering strips are important to increase bee species rich- habitat types show a relative similarity of different sites, but ness and abundance. also some contrasting patterns were found between the communities of different habitat types. The bee communities of Effect of habitat type on flower resources and bare cereal fields were highly dissimilar from bee communities soil in herbaceous strips and low-input meadows. Highest variability within a habitat type was found in herbaceous strips, There was a significant effect of habitat type on the number whereas variability was very low in low-input pastures. of flowering plant species (LM;F 4,40 = 24.72, p < 0.0001) and the flower cover (LM;F 4,40 = 44.23, p < 0.0001). High- est flowering plant species diversity and largest flower cover Discussion were found in low-input meadows, low-input pastures and flower strips (Table 4). The number of flowering plant spe- With 91 wild bee species recorded in the study area, a rela- cies was lowest in organic crop fields, but did not differ sig- tively high species diversity was found in this lowland agri- nificantly from flowering plant diversity of herbaceous strips cultural landscape of north-west Switzerland, reflecting a (Tukey-HSD, p = 0.2). The percent bare soil as a proxy of high landscape complexity. The records of 16 red-listed and nesting possibility differed between the habitat types (LM; 19 oligolectic species indicate the potential of these five F4,40 = 42.46, p < 0.0001). Low-input pastures contained the habitat types for bee conservation. Given that many habitat

Table 4 Flowering plant species Habitat type Flowering plant species Flower cover (%) Bare soil cover (%) (number), flower cover (%) and (number) amount of bare soil cover (%) in the different habitats using Low-input meadows 20.9 ± 1.0a 27.2 ± 2.1a 5.6 ± 0.7b GLMM Low-input pasture 20.3 ± 1.6a 19.6 ± 2.2ab 7.9 ± 1.9a Herbaceous strips 12.3 ± 0.9bc 10.7 ± 1.8b 1.3 ± 0.3c Flower strip 17.4 ± 1.6ab 28.5 ± 1.6a 1.9 ± 0.7c Organic cereal fields 8.6 ± 0.8c 1.6 ± 0.4c a

The difference between habitat types was analysed using multiple comparisons, with the post hoc “GLHT”. Different letters show significant differences a Cereal fields were excluded due to high disturbance by soil tillage resulting in a no-nesting habitat

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that bees are greatly influenced by flowering plant species and less by flower cover. But the abundance of oligolectic bee species was only significantly positively related to flower cover, and on the other hand red list species benefit more from flowering plant species. However, landscape context is just as important as site characteristics in determining bee community structure. A significant site variable in the AIC model may indicate the importance of the landscape in mediating bee species richness independently of the habitat variables measured. The parameter «site» was applied representing relevant aspects of landscape parameters in an aggregated form, because finally it was not possible to dis- tentangle different effects of landscape parameters. Since the study design did not allow a detailled landscape analysis. The bees complementarily responded in relation to habitat type: low-input meadows showed highest bee species richness and bee abundance compared to the other four habitat types. The bee species richness, however, did not differ Fig. 3 NMDS ordination comparing the different habitat types using a Bray–Curtis dissimilarity matrix of the bee abundance data; with between herbaceous strips and low-input meadows, despite a stress factor of 0.266. FLSt flower strips, LIP low-input pastures, a significantly lower number of flowering plant species and OCF organic cereal fields, HeSt herbaceous strips and LIM low-input a lower flower cover on the strips. This might account for meadows the fact that these strips offer different above ground nesting resources in the adjacent hedges, such as dead wood, specialists are unlikely to be found on managed farmland, plant stems. However, much higher bee abundances were these numbers are a substantial fraction of all potentially found in the low-input meadows and low-pastures and com- occurring species, with many European studies in agricul- pared to the strips and the cereal fields because these two tural landscapes only recording about 40–72 bee species, habitat types provide more food as pollen and nectar and e.g. in Sweden (Jönsson et al. 2015), England (Wood et al. nesting resources (e.g. a high percent bare soil). The much 2016) or France (Le Féon et al. 2013). This finding is in smaller area and width of herbaceous and flower strips and contrast to intensive agricultural landscapes in which the the higher disturbance in cereals by soil tillage may account number of common, highly mobile generalists were primar- for the lower number of bee species. Furthermore, highest ily boosted by habitat management (Winfree et al. 2009). number of flowering plant species and the percent bare soil Whereas low-input pastoral agriculture can maintain diverse found in both grassland types fostered wild bee populations. bee communities, especially if combined with semi-natu- Flower strips significant less positive impact on richness and ral habitat where vulnerable or endangered species have abundance of all wild bees, abundance of red list species a chance to survive (De Palma et al. 2015; Kremen and; and richness of oligolectic bees were found as shown in the M’Gonigle 2015). full model. All strip habitats are limited to enhance bees Wild bee species in dynamic agricultural landscapes can due to their relative small area size compared to large size benefit from semi-natural habitats such as permanent grass- grassland habitats . lands, hedgerows, pastures and woodland edges as they can In this study, we recorded 16 bumblebee species bene- provide critical feeding resources and nesting study sites fitting most from grassland habitats and flower strips, with for both above and below ground nesting species (Forrest 8 bumblebee species only found in grassland and flower et al. 2015; Garibaldi et al. 2011; Carrié et al. 2017). Our strip habitats. For species richness we found a significant results clearly show that bee species richness, bee abundance interaction of habitat type and flower cover and a strong and also subsets as the bumblebees and oligolectic species relation of habitat types to abundance and species rich- are greatly influenced by the habitat type. Habitat charac- ness (Table 2). Most bumblebee species are distinctly pol- teristics as number of flowering plant species and flower ylectic and mobile and therefore greatly benefit from the cover were identified as key-drivers, influencing bee popu- flower cover, independent of the habitat type, e.g. Bombus lations (Table 2). Surprisingly, the percentage of bare soil lapidarius and Bombus pascorum (Zurbuchen and Müller was not detected as a directly influencing variable in the 2012). Social bees as bumblebees are often dominant in full model based on AIC criterion. But we found a strong landscapes with low amounts and high fragmentation of significant effect on species richness and abundance of bees semi-natural habitats as grasslands and hedgerows (Carrié with increasing flowering plant species (Fig. 2). This shows et al. 2017), whereas solitary species were more sensitive

1 3 560 Journal of Insect Conservation (2018) 22:551–562 to the local loss of grassy permanent vegetation than social conditions for many wild bees (e.g. ground-nesting and species (Roulston and Goodell 2011). Our site (Möhlin) less mobile species). with the highest amount of intensive arable land had negatively influenced the bumblebees abundance compared to Community composition and species occurrence other sites confirming the findings of Carrié et al. (2017). Even though some crop fields can provide flowering The communities were dominated by solitary bee species resources for wild bees, such as mass-flowering crops representing 72% of all species recorded in the present study. (e.g. rape, sunflower) or weeds (Le Féon et al. 2013), Two highly abundant species were Lasioglossum malachu- farmed areas are likely seen to be as less suitable habitats rum (23.8% of the total sampling) and Halictus tumulorum for bee species such as grassland (Westphal et al. 2008). (12.2%). Both are ground nesting, polylectic and eusocial. Weed richness and cover are mostly decreasing with an Due to this form of sociality and the capacity to build two increasing farming intensity. However bees have been generations of worker bees per year enables them to be shown to move from semi-natural habitats into cropped highly reproductive (Strohm and Bordon-Hauser 2003). areas to forage on flowering resources (Holzschuh et al. NMDS-ordination analysis showed dissimilarities in bee 2008). We found the lowest species richness in organic species composition among the five habitat types with com- cereal fields, but not significantly different from that in munities in cereal fields, herbaceous strips and low-input low-input pastures and flower strips. However, with an pastures contrasting most. This suggests complementary average of 15 bee species and 6 endangered ones a diverse effects of different habitat types, which help to increase the wild bee fauna were found in this cereal habitat, charac- overall diversity of wild bees. Considering the different land- terised by a 1-year weed flora. This is in line with other use practices in the different habitats (e.g. grassland vs. pas- studies showing a relatively high bee (Holzschuh et al. tures) this may lead to a necessary, temporal mosaic of food 2007) and plant diversity (Clough et al. 2007) in organic resources offered to bees within their foraging range. The dif- cereal fields, especially in comparison with conventional ferences of landscape infrastructures between sites may have fields. Steffan-Dewenter and Tscharntke (2001) found on increased the variability of bee diversity within the habitat fallows that annual plants were visited more often by cer- type. Complementary perennial and annual low-input habi- tain bee families (Halictidae and Andrenida) than peren- tats promote wild bee diversity. However oligolectic species nial plants, suggesting that annual flowers in cereal fields were only found in habitats where their foraging plant species may represent important food resources for certain bee were present (e.g. on Campanula specialised, endangered species (Holzschuh et al. 2008). Two red list species and bees as Andrena pandellei, A. curvungula, Lasioglossum cos- four polylectic species were only recorded in these cere- tulatum). This shows that these specialists are less dependent als. These included a highly endangered, oligolectic spe- directly by a specific habitat type and species richness of cies Colletes similis, which is specialized on Asteraceae dicots in general. Specialised bee species adapted to particu- and might have collected pollen on annual Matricaria sp., lar plant species, or requiring specific nesting resources tend recorded in these cereals. The exclusive occurrence of six to be more vulnerable to landuse changes than polylectic, species underlines the relevance of this arable crop habi- generalised species (Potts et al. 2003; Kovács-Hostyánszki tat for the conservation of certain bee species (Table S4). et al. 2017). Red list bee species were found to be much more The cereal fields were (in comparison with perennial influenced by the site than habitat types. Increasing num- habitats) less diverse in food plants, highly disturbed by ber of flowering plants positively influenced red-list species farm practices (e.g. harvesting, soil tillage) and rarely (Table 4; Fig. S8). But our findings that 31 wild bee species offered microhabitats for nesting, making them primarily were only recorded in one habitat type (including seven red- food rather than nesting habitats. But organic cereal fields listed and four oligolectic species) indicates a complementary offer a high abundance of weeds such as wild chamomile benefit of each habitat type. (Matricaria chamomilla) and other flowering annual dicots The effectiveness of wild bee supporting practices by (e.g. Polgonum sp., Centaurea cyanus, Sinapis arvensis) habitat management is influenced by interactive effects in contrast to the plant communities of grassland habitats between small and large scale factors. With increasing land which were dominated by biannual and perennial plants use intensity, species with higher environmental require- (Table S9). Only at untilled field edges can wild bees find ments, such as specialised, oligolectic species are disappear- nest sites nearby. Therefore, cereals offer completely dif- ing first (Rader et al. 2014). Moreover the amount of arable ferent conditions with an annual arable flora compared land may negatively alter the occurrence of certain wild bee to perennial low-input habitats. However, the perennial, species (e.g. B. pascuorum, L. lativentre and L. calceatum; unfertilized habitats, only cut 1–2 times per year, offer a Table S3), and Knight et al. (2009) also found a negative long period of flower resources leading to more suitable correlation with bumblebee abundance and the amount of arable land. However, we found some complementary effects

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