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 habi- tats, 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/s1084 1-018-0084-6) 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).