Sown wildflower strips as overwintering habitat for arthropods: Effective measure or ecological trap?

Agriculture, Ecosystems and Environment 275 (2019) 123–131

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Sown wildflower strips as overwintering habitat for arthropods: Effective measure or ecological trap?

T

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Dominik Gansera,b, , Eva Knopa, Matthias Albrechtb a b

University of Bern, Institute of Ecology and Evolution, Baltzerstrasse 6, 3012, Bern, Switzerland Agroscope, Agroecology and Environment, Reckenholzstrasse 191, Zürich, 8046, Switzerland

A R T I C LE I N FO

A B S T R A C T

Keywords: Agri-environment schemes Biological control Ecological trap Emergence trap Flower strip Insect hibernation

Wildflower strips (WFS) are increasingly commonly adopted measures to promote biodiversity in agro-ecosystems. While their effectiveness in providing floral and other food resources for pollinators and natural enemies has been relatively well studied, much less is known about the value of different types of WFS as overwintering habitat for different functional arthropod groups. Here, we examined arthropod overwintering in WFS of different age compared to winter wheat fields. Moreover, we addressed the largely unexplored question to what extent non-permanent WFS may act as sink or ecological trap, if they attract high numbers of overwintering arthropods but only a low proportion of them survive and successfully emerge due to ploughing of strips during overwintering. Overwintering of all studied arthropod groups eincluding potential pest natural enemies spiders, carabid beetles, staphylinid beetles and different families of pollinating flies ewas higher in WFS compared to winter wheat crops. Overwintering increased in WFS compared to wheat fields irrespective of WFS age, except for 4 year old WFS in the case of carabid beetles and 1 year old WFS in the case of spiders. While WFS age positively affected spider overwintering, numbers of overwintering pollinating flies and staphylinid beetles did not change significantly with WFS age. Moreover, carabid beetles tended to decline in the four years old WFS compared to younger ones. Ploughing of annual WFS during overwintering significantly reduced the number of successfully emerging arthropods by 59% on average. Detrimental effects were strongest for carabid beetles and spiders (reductions by 67% and 69%, respectively) to their numbers in ploughed WFS being similar to winter wheat fields. Reductions were less severe for pollinating flies and staphylinid beetles (both 47%), with higher numbers emerging from annual WFS compared to winter wheat fields even after ploughing of WFS. We conclude that perennial WFS are valuable overwintering habitats for a range of arthropod taxa across functional groups in arable cropping systems. Distinct responses of different arthropod taxa to WFS age highlight the importance of managing perennial WFS of various successional stages in order to promote overwintering of a broad variety arthropods in agro-ecosystems. Our study raises concerns, however, that annual WFS ploughed during the overwintering period are poor overwintering habitats for arthropods and may even act as ecological traps.

1. Introduction In most regions of the world increasing demand for agricultural production for a growing population have led to an expanded cultivation of crops at the cost of semi-natural habitats in agro-ecosystems (FAOSTAT, 2016). The loss of these habitats, along with intensified agricultural practices, has caused a decline in farmland biodiversity and ecosystem services, including crop pollination (Kennedy et al., 2013; IPBES 2016) and natural pest control services (Tscharntke et al., 2005; Veres et al., 2013).

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In the last decades, considerable effort has been undertaken to mitigate the loss of biodiversity and associated ecosystem services in agroecosystems (e.g. Ekroos et al., 2014). In the framework of the common agricultural policy of the European Union, for example, greening measures including the implementation of ecological focus areas, i.e. specified types of preserved or newly created green infrastructure and semi-natural habitats, are promoted (European Union, 2014). Wildflower strips (hereafter WFS) are increasingly commonly established as ecological focus areas in Europe, but also as restoration measures in many other regions of the world, to promote farmland

Corresponding author. E-mail addresses: [email protected] (D. Ganser), [email protected] (E. Knop), [email protected] (M. Albrecht).

https://doi.org/10.1016/j.agee.2019.02.010 Received 12 November 2018; Received in revised form 9 February 2019; Accepted 12 February 2019 0167-8809/ © 2019 Elsevier B.V. All rights reserved.

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overwintering considering both local and landscape drivers are scarce. Here, we address the following specific research questions: (i) Do WFS enhance number of emerging arthropods compared with arable crops? (ii) How do local WFS traits and landscape context affect the number of emerging arthropods in WFS? (iii) How do numbers of overwintering arthropods change with age of WFS (1–4 years)? (iv) Can annual WFS act as ecological traps for overwintering arthropods?

biodiversity (reviewed e.g. in Haaland et al., 2011; Scheper et al., 2013). The implicit or explicit goal of WFS is to promote in particular a range of beneficial arthropods contributing to the provision of ecosystem services, such as crop pollination or natural pest control (Wäckers and van Rijn, 2012; Wratten et al., 2012). In fact, a series of studies have shown that WFS can contribute to natural pest control (Blaauw and Isaacs, 2015; Sutter et al., 2018a; Tschumi et al., 2016a) and pollination services in nearby crops (Balzan et al., 2016; Blaauw and Isaacs, 2014; Ganser et al., 2018; Venturini et al., 2017). A prerequisite for such positive functional spillover effects from WFS to crops (Blitzer et al., 2012) is that WFS need to effectively provide pollinators and natural enemies with vital resources they rely on during their life cycle, including nectar and pollen, alternative prey, shelter from disturbance and overwintering habitat (Haaland et al., 2011; Wäckers and van Rijn, 2012; Wratten et al., 2012). The vast majority of studies have investigated the role of floral food resources in locally promoting pollinator and natural enemy abundance and diversity, generally finding positive relationships between floral resource abundance and diversity with the abundance and/or diversity of beneficial arthropods (e.g. Balzan et al., 2016; Scheper et al., 2013; Sutter et al., 2017; Tschumi et al., 2016a, 2015; Wäckers and van Rijn, 2012). Much less is known about the effectiveness of different types of WFS as overwintering habitat for pollinators and natural enemies (but see e.g. Frank and Reichhart, 2004; Sutter et al., 2018b), despite its crucial role for the long-term persistence of populations of beneficial insects in agro-ecosystems (e.g. Aviron et al., 2007; Carvell et al., 2007; Woodcock et al., 2008). In arable crop dominated agro-ecosystems WFS may be potentially important overwintering habitats for arthropods overwintering in the soil, as soils are relatively undisturbed, in contrast to those of intensively managed and conventionally tilled arable crops. The potential of WFS as overwintering habitat for arthropods may, however, depend on the type and age of the WFS due to successional changes in vegetation and soil properties over time (Frank and Reichhart, 2004). Such properties may include the proportion of bare soil, plant species composition and diversity or soil characteristics such as bulk density (McCabe et al., 2017; Sarthou et al., 2014; Sutter et al., 2018b). Such successional changes in overwintering habiat properties along with the absence of disturbance by farming activities over the years may favour overwintering of arthropods (Frank and Reichhart, 2004; Pfiffner and Luka, 2000) resulting in a positive linear or saturating relationship between WFS age and overwintering of arthropods (Frank and Reichhart, 2004). However grassy vegetation often starts to dominate WFS after two to three years, potentially reducing overwintering habitat quality for some arthropod groups in old WFS (Günter, 2000). Thus, a hump-shaped relationship between WFS age and overwintering of arthropods could be hypothesized. WFS are generally annual in rotation with crops, or they are perennial and in place up to several years before they are ploughed. Ploughing is expected to have severe negative impacts on emergence rates of beneficial arthropods overwintering in the soil (Pfiffner and Luka, 2000; Ullmann et al., 2016). Thus, a putative attractive overwintering habitat may become a sink or ecological trap, if it attracts high numbers of overwintering arthropods but only a low proportion of them survive due to ploughing of strips during overwintering. However, to our knowledge, the effect of ploughing of WFS and their possible role as ecological traps in terms of overwintering remains unexplored. Thus, we do not know if WFS support only short-term persistence of beneficial arthropods in agricultural landscapes, or if they also promote beneficial arthropods on a population level. The success of agri-environmental measures, such as WFS, in promoting beneficial arthropods may not only depend on the local WFS properties and their temporal dynamics, but also on surrounding landscape. For example, semi-natural habitats provide source populations of beneficial arthropods to colonize WFS (Jonsson et al., 2015; Tscharntke et al., 2016). However, studies investigating arthropod

2. Materials and methods 2.1. Study design A total of 28 sites were randomly chosen in the central Swiss plateau (cantons Bern, Zurich, Solothurn and Aargau). The study region (ca. 34 × 133 km) is characterized by typical Swiss agricultural landscapes consisting of arable crops, grasslands and forest patches in a relatively small-scaled mosaic. The minimum distance between sites was 3 km. Each site was either a WFS established adjacent to a winter wheat field or a winter wheat field without adjacent WFS serving as independent control habitat, i.e. reflecting the situation without establishment of WFS; only narrow grassy strips bordered these wheat fields (see Appendix Fig. A1 for a graphical illustration of the local sampling design). The size of the adjacent strips ranged from 0.048 to 2.7 ha (mean: 0.8 ha). Wheat fields were managed according to a commonly practiced IPM production system in Switzerland (following the “Extenso” guidelines of the IP Suisse label organization): e.g. synthetic fertilizer applications and herbicides are allowed, but not the use of insecticides. In 2016 and 2017, arthropods emerging from overwintering were sampled in WFS and winter wheat fields (≥ 3 km apart from each other, see above). At the time of sampling, WFS were of different age (i.e. years or vegetative growth seasons and overwintering periods since their establishment). Specifically, in 2016, arthropods emerging from overwintering were sampled in eight WFS sown in autumn 2015 (sampling of arthropods emerging from the first overwintering period since the establishment of the WFS: year 1), six WFS sown in spring 2013 (third overwintering period: year 3) and eight independent winter wheat fields serving as control sites. In 2017, six WFS sown in spring 2016 (year 2), the same six perennial WFS sown in 2013 (year 4), as well as the same winter wheat control sites were sampled. Moreover, to test the effect of ploughing of WFS, half of the area of four of the six WFS sown in spring 2016 was ploughed in December 2016, while the other half of the same WFS remained untreated (Appendix Fig. A1). WFS consisted of annual and perennial mainly wild native and some cultivated flowering plant species, which were primarily selected, based on high pollen and nectar rewards for flower-visiting insects (see Appendix Table A1 for a detailed description of WFS seed mixtures). Each WFS had a width of 6 m and had a minimum length of 80 m. For detailed descriptions of sown plant species, selection criteria for inclusion in a seed mixture and management prescriptions of WFS see Tschumi et al. (2016a) and Ganser et al. (2018). 2.2. Sampling of overwintering arthropods Emergence traps (photoeclectors) were used to capture arthropods emerging from the soil and leaf litter layer from overwintering (Sarthou et al., 2014; Sutter et al., 2018b). Emergence traps consisted of a solid metal frame (50 × 50 cm) dug 10 cm deep into the soil, covered with a dark mesh fixed on a pyramid-like metal structure (Sutter et al., 2018b). Each emergence trap contained a killing jar filled with a 25% propandiol solution fixed to below the top of the pyramid-like frame of the trap to catch flying arthropods emerging from overwintering. Additionally, a pitfall trap (plastic cup, 6.5 cm diameter and 12.5 cm deep, half filled with a 25% propoandiol solution and a scentless detergent to decrease water surface tension) was inserted into the ground in one corner of the trap to catch epigeous arthropods. Traps were placed in the beginning of March and emptied every three weeks until the end of 124

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to a model without the random observation parameter. In case the observation-level random factor significantly improved the model, it was remained in the model (Bolker et al., 2009). Tukey’s post-hoc tests for multiple comparisons were used to test for significant differences among factor levels using the multcomp package (version 1.3–6; Hothorn et al.,2014). To assess to what extent annual flower strips may act as ecological traps for overwintering arthropods we quantified differences in the number of arthropods overwintering and successfully emerging from overwintering in (i) 1-year-old undisturbed WFS (6 sites); (ii) flower strips ploughed after the growth period in late October 2016 (which represents the standard ploughing date of annual flower strips in the study region; 4 sites) and (iii) winter wheat fields (8 sites). Differences in the higher number of arthropod individuals overwintering in treatment (i) (undisturbed WFS) and (iii) (wheat field) indicates how many more individuals prefer to overwinter and emerge from overwintering in spring-sown WFS compared to wheat fields, whereas the difference between treatment (i) and (ii) reflects the extent to which ploughing of WFS at the end of the year reduces the number of arthropods emerging from overwintering. Treatment effects on emerging arthropod numbers (for each arthropod group separately; pooled numbers of individuals during the emergence sampling period) were modeled with GLMMs with a Poisson error distribution using treatment as fixed factor with the three treatment levels i, ii and iii, and site as a random factor. Tukey’s post hoc tests were used to test for significant differences among treatment levels. In addition to treatment, the percentage of semi-natural habitats and the percentage of crops in the surrounding landscape (500 m radius) were included as fixed factors in the models. All numerical explanatory variables were standardized (scaled) prior to the analyses. All analyses were done in R version 3.2.1 (R Core Team, 2017), using the lme4 package (Bates et al., 2015).

June in both sampling years (2016 and 2017). Four traps were used at each treatment site (i.e. winter wheat field control, flower strip of different age, ploughed or not): two traps at 1 m and two traps at 3 m from the border of the sampled habitat (see Appendix Fig. A1). Individuals of the following taxonomic groups were counted: pollinating flies (Diptera), spiders (Araneae), carabid beetles (Carabidae) and staphylinid beetles (Staphylinidae). Spiders, carabid and staphylinid beetles are known as key predators of many crop pests (e.g. Alford et al., 2003; Holland et al., 2008), whereas the fly families Empidiae, Anthomyiidae, Platystomatidae, Tachinidae, Scatophagidae, Syrphidae and Tipuloidae have been identified as potential pollinators of crops and wild plants (e.g. Orford et al., 2015). The total number of carabid beetles was used as a proxy of predatory carabid beetles in the analysis, as number of predatory carabid beetle is usually highly positively correlated with the total number of carabid beetles (e.g. Sutter et al., 2018a). 2.3. Local vegetation characteristics and landscape context In each sampling location within each site, the percentage of bare ground cover and plant species richness (i.e. the total number of plant species per plot) were quantified within a radius of one metre around the traps, at each of the three-week sampling rounds described above. We focused on these two local vegetation characteristics because they have been identified as potential key drivers of arthropod overwintering in previous studies (e.g. McCabe et al., 2017; Sarthou et al., 2014; Sutter et al., 2018b) and because they represent simple characteristics for different types and successional stages of WFS that can be readily assessed and communicated to farmers interested in improving the potential of their WFS with respect to beneficial arthropod overwintering. Furthermore, we quantified the percentage of semi-natural habitats (i.e. extensively managed grassland, wildflower areas, ruderal areas, hedges, woodlands) as a proxy of landscape complexity (Tscharntke et al., 2005) in a landscape sector of 500 m radius around each study site (Sarthou et al., 2014). Additionally, the percentage of crops (e.g. oilseed rape, wheat, potatoes) as a proxy of landscape simplification (Tscharntke et al., 2005) were quantified using existing maps available as GIS layers (TLM3D, swisstopo, Wabern). The calculations were performed using ArcMap 10.1 GIS software.

3. Results 3.1. Arthropod overwintering in wheat fields and WFS of different age A total of 7009 arthropod individuals were sampled with the emergence traps, including 1502 flies, 2161 carabid beetles, 1928 spiders and 1418 staphylinid beetles. The number of successfully overwintering flies and staphylinid beetles was higher in WFS than in winter wheat fields, irrespective of the WFS age (Table 1a; Fig. 1), with average increases of 77.63% and 83.67%, respectively. Average numbers of carabid beetles and spiders were also higher in WFS compared to winter wheat fields, but differences were only statistically significant for the 1–3 years old WFS for carabid beetles (58.93% increase), and the older (2–4 years) WFS in the case of spiders, respectively with 81.69% more overwintering spiders in these older WFS compared to winter wheat fields (Fig. 1). Numbers of successfully emerging flies or staphylinid beetles did not significantly differ between flower strips of different age (1–4 years; Fig. 1). Numbers of overwintering spiders, however, were higher in the 3–4 years old WFS than in the 1–2 years old WFS (Fig. 1).

2.4. Data analysis First, we tested differences in the number of emerged overwintering individuals of each of the investigated arthropod group between wheat crop fields and WFS of different age with a generalized linear mixed effects (GLMM) models assuming a Poisson error distribution. The fixed explanatory variable was overwintering habitat (factor with five levels: wheat field, WFS of age 1, 2, 3 or 4), and site and study year were included as nested random effects (random intercept models). Individuals of emerged pollinating flies, carabid beetles, spiders and staphylinid beetles captured in each trap were summed over the sampling period. We then examined the role of local and landscape drivers of arthropod overwintering across WFS of different age (1–4 years), using GLMMs assuming a Poisson error distribution. Explanatory variables were WFS age (factor, age class 1–4), percentage bare soil, plant species richness (averaged across sampling locations per site), emergence trap location (1 m or 3 m from border) and the percentage of semi-natural habitat and crops around sites (500 m radius) as fixed effects and site and study year were included as nested random effects (random intercept models). No interaction terms were included to avoid overfitting of the models. Potential co-linearity among explanatory variables was assessed, but none of the explanatory variables were strongly correlated (r < 0.6; Zuur et al., 2009). All GLMMs were also checked for overdispersion by including an observation-level random factor (level of observations) into the model and comparing it

3.2. Local and landscape factors affecting arthropod overwintering in WFS of different age Local habitat characteristics had no effect on staphylinid beetles (Table 1b); however the percentage of bare soil negatively affected the number of emerging flies and spiders (Table 1b). Moreover, the number of emerging carabid beetles increased with plant species richness (Table 1b). Neither the amount of semi-natural habitats nor the proportion of crops in the landscape surrounding of the study sites significantly impacted the number of overwintering, emerging arthropods (Table 1b). 125

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Table 1 Results of generalized linear mixed effects models to test for (a) differences between wheat fields (Intercept) and WFS of different age (factor with five levels: wheat field, WFS of year 1, 2, 3 or 4 with undisturbed overwintering), and (b) to test for effects of percentage of semi-natural habitats (% SNH) and percentage of crops (% crops) in the surrounding of 500 m around focal WFS, percentage of bare soil (% bare soil) of local WFS, location of traps within local WFS (wheat fields, respectively) (centre and edge), and WFS of different age (1,2,3 and 4 years with undisturbed overwintering) on numbers of emerging overwintering arthropods across studied groups (pollinating Diptera, Carabidae, Araneae, Staphylinidae). Random effects: 1|site id/year. Estimate of the respective variable in the final model (estimate), estimate standard error (SE), z-value (Z) and P-value (P:significant P-values (< 0.05) are shown in bold). Diptera

Response: Overwintering numbers (a) wheat field (Intercept) year 1 year 2 year 3 year 4 (b) year 1 (Intercept) year 2 year 3 year 4 % crops % SNH % bare soil plant species richness location (edge)

Carabidae

Araneae

Staphylinidae

Estimate

SE

Z

P

Estimate

SE

Z

P

Estimate

SE

Z

P

Estimate

SE

Z

P

−2.01 2.05 2.30 2.13 2.10

0.18 0.23 0.26 0.25 0.27

−10.91 9.08 8.94 8.39 7.66

< .001 < .001 < .001 < .001 < .001

−2.03 0.68 0.59 1.02 0.56

0.24 0.31 0.35 0.35 0.39

−8.33 2.20 1.66 2.89 1.45

< .001 0.028 0.097 0.004 0.147

−1.99 1.52 1.83 2.39 2.49

0.19 0.23 0.26 0.26 0.28

−10.61 6.51 7.01 9.27 9.02

< .001 < .001 < .001 < .001 < .001

−2.81 2.19 2.35 2.75 2.47

0.22 0.26 0.28 0.28 0.30

−12.79 8.44 8.29 9.72 8.16

< .001 < .001 < .001 < .001 < .001

−0.83 −0.38 −0.21 −0.46 0.14 −0.21 −1.64 0.08 −0.15

0.37 0.28 0.25 0.27 0.25 0.22 0.88 0.03 0.15

−2.24 −1.36 −0.86 −1.70 −0.09 −0.93 −1.86 2.33 −1.04

0.025 0.173 0.388 0.089 0.586 0.351 0.062 0.019 0.298

−3.33 −1.11 0.21 −0.61 0.46 0.25 −1.94 0.15 0.48

0.76 0.56 0.47 0.54 0.50 0.45 1.57 0.07 0.30

−4.40 −1.97 0.45 −1.14 0.93 0.55 −1.23 2.28 1.58

< .001 0.049 0.649 0.253 0.351 0.585 0.217 0.022 0.113

−1.90 −0.28 0.67 0.63 0.06 0.32 −3.01 0.05 0.01

0.47 0.32 0.27 0.30 0.28 0.26 1.02 0.04 0.17

−4.06 −0.88 2.53 2.11 0.22 1.26 −2.94 1.46 0.07

< .001 0.378 0.012 0.035 0.829 0.209 0.003 0.144 0.946

−1.08 −0.16 0.26 −0.10 0.05 −0.35 −1.02 0.04 −0.03

0.49 0.37 0.30 0.35 0.32 0.30 1.04 0.04 0.19

−2.21 −0.45 0.97 −0.28 0.14 −1.93 −0.98 0.86 −0.17

0.028 0.654 0.349 0.782 0.887 0.232 0.330 0.389 0.863

activity densities of different spider families during the growing period in fallow strips. For example, Lycosidae and Araneidae spiders substantially increased in grass and wildflower strips over three years, while the number of Linyphiidae remained relatively stable over the this time period. Whether similarly distinct temporal patterns across spider families may also be observed for overwintering spiders remains to be tested. Carabid beetles showed maximum overwintering densities after 2–3 years, which is in line with findings by Frank and Reichhart (2004). The observed decline of carabid overwintering in WFS from the third to fourth year might be driven by a shift in vegetation cover from herbaceous plant dominated vegetation to grass dominated vegetation generally observed during this time period (Günter, 2000; Ganser, unpublished data) that could turn WFS into less favorable overwintering habitats for carabid beetles (Pywell et al., 2005). However, carabid beetles have been found to prefer margins with tussock forming grasses (Woodcock et al. 2010), but this type of grassy vegetation was not common in the WFS studied here. It is important to note that by using emergence traps rather than soil sampling, as many previous studies (e.g. Frank and Reichhart, 2004; Geiger et al., 2009; Pfiffner and Luka, 2000), we were able to measure the number of emerging insects that have successfully overwintered in a habitat rather than the overwintering habitat preference of arthropods. Our emergence measures are particularly relevant in terms of the potential of WFS to enhance pest control and pollination services delivered by overwintering arthropods that actually emerge in spring (e.g. Mestre et al., 2018; Sutter et al., 2018a).

3.3. Do annual WFS act as ecological traps for overwintering arthropods? Ploughing of WFS at the end of the year significantly reduced the number of successfully overwintering arthropods by 59.04% on average compared to WFS left undisturbed across all studied arthropod groups (Fig. 2). Detrimental effects were strongest for carabid beetles and spiders (reductions by 67% and 69%, respectively) to their numbers in ploughed WFS being similar to winter wheat fields. Reductions were less severe for pollinating flies and staphylinid beetles (47.41% and 47.04%, respectively), with higher numbers emerging from annual WFS compared to winter wheat fields even after ploughing of WFS (Table 2, Fig. 2). 4. Discussion 4.1. Arthropod overwintering in wheat fields and WFS of different age The present study shows that significantly more arthropods across different taxonomic groups, including potential providers of pest control and pollination services, successfully overwinter in WFS compared to winter wheat, which is in a line with findings of Lys and Nentwig (1994); Pfiffner and Luka (2000) and Frank and Reichhart (2004). Moreover, our findings indicate that the value of WFS as overwintering habitat for different taxonomic groups of arthropods depends on WFS age. However, unlike Frank and Reichhart (2004) who reported an increase of overwintering of carabid and staphylinid beetles up to the third year after WFS establishment, we found distinct successional changes of different arthropod groups over time. While WFS age positively affected spider overwintering, with more spiders overwintering in 3–4 years old WFS, numbers of overwintering flies and staphylinid beetles did not change significantly with WFS age. Overwintering carabid beetles declined in the oldest, four years old WFS compared to younger ones. Thus, our findings suggests that, in an agricultural landscape, WFS of different age and successional stage may be required to ensure optimal overwintering conditions across multiple taxonomic groups of arthropods. Spiders in particular appear to benefit in terms of overwintering from the long-term absence of soil management and the vegetation and soil conditions associated with older WFS (Mestre et al., 2018). Toivonen et al. (2018) found distinct temporal dynamics of

4.2. Local and landscape factors affecting arthropod overwintering in WFS of different age Our findings indicate that overwintering of the studied groups of flies as well as spiders in WFS was positively associcated with vegetation cover, while negatively affected by high percentages of bare soil. These results are in accordance with those for other semi-natural habitats in agricultural landscapes, such as permanent grassland, hedgerows or forest edges (Mestre et al., 2018; Sarthou et al., 2014; Frank and Reichhart (2004). More dense vegetation cover can have favorable effects due to better insulation and less frequent and severe frosts that could harm soil-overwintering arthropods (Sotherton, 1984; Thomas 126

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Fig. 1. The abundance of the arthropod groups (a) pollinating Diptera, (b) Carabidae, (c) Araneae, and (d) Staphylinidae dependent on the habitat (0: winter wheat control field) and age of the WFS (1–4 years with undisturbed overwintering). Different letters represent significantly different means at p ≤ 0.05.

et al., 1991). Interestingly, fly and caribid beetle overwintering was also positively influenced by high plant diversity in WFS. Therefore, they do not only offer food resources to pollinators (Balzan et al., 2016; Ganser et al., 2018; Scheper et al., 2013) and are a valuable habitat to natural enemies of pest species (e.g. Sutherland et al., 2001; Tschumi et al., 2016a), but may also be a preferred high quality habitat for overwintering. This could be due to an increased structural diversity and heterogeneity of the vegetation in plant species rich WFS (Frank and Künzle, 2006; Geiger et al., 2009; Schellhorn and Sork, 1997; Woodcock et al., 2005), enhancing overwintering habitat quality for these arthropod groups. Diverse vegetation may also offer more suitable habitat during the growing season for these arthropod taxa, increasing the probability that they choose it later on also as overwintering habitat. In contrast to these local drivers of arthropod overwintering in WFS, landscape-level factors, such as the proportion of crops or semi-natural habitats in the surrounding of the WFS had no detectable direct effect on arthropod overwintering in our study. This corroborates recent findings by Sarthou et al. (2014) and Sutter et al. (2018a), suggesting that local rather than landscape factors are the major drivers of arthropod overwintering in agro-ecosystems.

4.3. Do annual WFS act as ecological traps for overwintering arthropods? A currently largely neglected, but a potential key aspect of WFS and other types of plantings in place for a limited time to promote beneficial arthropods is the impact of the ploughing on arthropod overwintering. In the present study we have measured the result of both overwintering habitat preference and successful overwintering showing that annual WFS are indeed valuable overwintering habitats for a range of arthropod taxa (see also 4.1), corroborating evidence by Pfiffner and Luka (2000) or Frank et al. (2007). Moreover, our findings clearly show a pronounced decrease in emergence across all studied arthropod groups in WFS ploughed during the overwintering period compared to undisturbed WFS. The observed variation in detrimental effects between arthropod groups might be due to variation in soil depth the different taxa overwinter or other taxa-specific life-history traits, such as the life history stage in which they overwinter, contributing to their vulnerability to tillage in this stage. Unfortunately, we cannot provide specieslevel information with respect to the ability of arthropods to survive ploughing, which should be addressed in future studies to better understand how ploughing may affect community compositions of successfully emerging arthropods based on their overwintering and relevant life-history traits (e.g. Holland et al., 2016). Nevertheless, to our

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Fig. 2. The abundance of the arthropod groups (a) pollinating Diptera, (b) Carabidae, (c) Araneae, and (d) Staphylinidae in the different treatments: WFS (annual wildflower strips with undisturbed overwintering period), ploughed WFS (annual wildflower strips ploughed during overwintering period) and control fields (winter wheat fields). Different letters represent significantly different means at p ≤ 0.05.

knowledge, our study is among the first addressing to what extent annual WFS may act as ecological traps for arthropods. Annual WFS can be highly effective in providing pollinators and pests’ natural enemies with food resources, potentially promoting their fitness and the local delivery of associated crop pollination and pest control services (e.g. Jonsson et al., 2015; Lee and Heimpel, 2008;

Tschumi et al., 2016b, 2015). The value of such measures in terms of overwintering habitat to promote arthropod populations in the long term, however, should also be considered. Moreover, the risk of WFS to become ecological traps or sink habitats should be minimized. From this perspective, perennial WFS ensuring undisturbed overwintering during at least one overwintering period are strongly recommended.

Table 2 Results of generalized linear mixed effects models to test for effects of ploughing of annual WFS during the overwintering period compared to undisturbed annual WFS and winter wheat control fields on overwintering arthropod groups (pollinating Diptera, Carabidae, Araneae, Staphylinidae). Models included the covariates percentage of SNH (% SNH) and percentage crops (% crops) in the surrounding of 500 m. Random effects: 1|site id. Estimate of the respective variable in the final model (estimate), estimate standard error (SE), z-value (Z) and P-value (P:significant P-values (< 0.05) are shown in bold). Diptera

Response: Overwintering numbers undisturbed WFS (Intercept) ploughed WFS control wheat fields % SNH % crops

Carabidae

Araneae

Staphylinidae

Estimate

SE

Z

P

Estimate

SE

Z

P

Estimate

SE

Z

P

Estimate

SE

Z

P

0.25 −0.57 −2.13 −0.33 0.15

0.1 0.2 0.3 0.3 0.2

1.77 −2.61 −7.22 −1.32 0.59

0.077 0.009 < .001 0.188 0.558

0.12 −1.16 −1.54 −0.61 −0.45

0.2 0.3 0.4 0.4 0.4

0.47 −3.38 −3.63 −1.61 −1.13

0.64 < .001 < .001 0.111 0.261

−1.53 −1.12 −1.26 0.03 0.69

0.4 0.5 0.5 0.5 0.5

−3.94 −2.43 −2.42 0.06 1.35

< .001 0.015 0.016 0.949 0.176

−0.39 −0.51 −2.61 −0.76 0.45

0.2 0.3 0.3 0.3 0.3

−2.18 −1.78 −7.44 −2.71 1.41

0.029 0.075 < .001 0.007 0.159

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However, also perennial WFS are generally ploughed after a couple of years due to a loss of flowering herbaceous plants replaced by increasingly dominant invading grasses and an associated loss of floral resource provisioning for flower-visiting insects (e.g. Günter, 2000; Ganser, unpublished data). As arthropods seem to overwinter in higher numbers in relatively old WFS (in particular spiders in this study, see also Frank and Reichhart, 2004) losses are likely also higher in the year these strips are ploughed. Nevertheless, the beneficial effects of several years of undisturbed overwintering on arthropod populations should by far exceed the adverse effects of such losses in the year of ploughing. However, to our knowledge, quantitative data and robust predictions of the impacts of different ploughing regimes on long-term arthropod community dynamics are currently lacking.

promote overwintering of a broad variety of arthropods in agro-ecosystems. Our findings suggest that WFS should consist of a diverse, relatively dense vegetation to enhance their potential as overwintering habitat for arthropods. Our study raises concerns, however, that annual WFS ploughed during the overwintering period are poor overwintering habitats for arthropods and may even act as ecological traps. More research on the impact of such effects on the long-term population dynamics of arthropods in agro-ecosystems is needed.

5. Conclusions

Acknowledgments

Our study shows that perennial WFS are valuable overwintering habitats for a range of arthropod taxa across functional groups in arable crop-dominated agricultural landscapes. Distinct responses of different arthropod taxa to perennial WFS of different age highlights the importance of perennial WFS of various successional stages in order to

We are grateful to two anonymous reviewers for their insightful comments and revisions, and to Debora Unternährer, Alexandra Glauser, Laura Dällenbach, Paul-Emile Desaulles and Stephan Bosshart for all their help in the lab and the field. We owe special thanks to the local farmers for granting us the use of their properties.

Funding This study was financed by the Swiss Federal Office for Agriculture (BLW).

Appendix A See

Table A1 Seed mixtures of WFS. Mixture 1 was sown in autumn 2015 and 2016, mixture 2 in spring 2016. See Materials and methods for a detailed description of the study design. Seed mixtures Mixture 1 (2015) Anethum graveolens Campanula patula Campanula rapunculoides Centaurea scabiosa Centaureus cyanus Centaureus jacea Cichorium intybus Clinopodium vulgare Consolida regalis Crepis biennis Crepis capillaris Daucus carota Fagopyrum esculentum Hypochaeris radicata Knautia Arvensis Lamium purpureum Linum usitatissimum Malva sylvestris Origanum vulgare Papaver rhoeas Phacelia tanacetifolia Reseda lutea Scabiosa columbaria Sinapsis arvensis Stachys annua Stachys officinalis Melilotus albus Onobrychis viciifolia Trifolium pratense Anchusa arvensis Anthemis tinctoria Camelina sativa Echium vulgare Leontodon hispidus Lotus corniculatus Picris hieracioides Trifolium hybridum Trifolium incarnatum Vicia sativa

x x x x x

Mixture 2 (2016)

x x x x x x x x x x x x x x x x x x x x x x x x x x x x

x

x x x

x

x x x x x x x x x x x x x x x x x

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Fig. A1. Schematic study and local sampling design. Emergence trap location in a) WFS (light grey coloured area) adjacent to winter wheat field, b) winter wheat control field; c) study and sampling design to test the effect of ploughing of annual flower strips: half of the WFS area was ploughed and the other remained undisturbed (emergence trap sampling in winter wheat control fields not shown); d) two emergence traps in a WFS. Dark grey-coloured area: narrow grassy strips typically bordering wheat fields in the study region.

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