ALTERRA ALTERRA Promoting wild bees in European agricultural landscapes agricultural Promoting wild bees inEuropean Promoting wild bees in European SCIENTIFIC CONTRIBUTIONS agricultural landscapes The role of floral resources in driving and mitigating wild bee decline Jeroen Alexander Scheper 47 Jeroen Alexander Scheper Promoting wild bees in European agricultural landscapes The role of floral resources in driving and mitigating wild bee decline Jeroen Alexander Scheper The research presented in this thesis was conducted at Alterra in Wageningen, The Netherlands Alterra, Wageningen University & Research Centre, 2015 Alterra Scientific Contributions 47 Scheper, J.A. 2015. Promoting wild bees in European agricultural landscapes. The role of floral resources in driving and mitigating wild bee decline. Alterra, Wageningen University & Research Centre, Wageningen. Omslag: Wageningen UR, Communication Services Illustraties omslag: Timon, Emma en Linde Scheper Layout: Jeroen Scheper Drukwerk: Wageningen UR, Communication Services Promoting wild bees in European agricultural landscapes The role of floral resources in driving and mitigating wild bee decline Proefschrift ter verkrijging van de graad van doctor aan de Radboud Universiteit Nijmegen op gezag van de rector magnificus prof. dr. Th.L.M. Engelen, volgens besluit van het college van decanen in het openbaar te verdedigen op vrijdag 18 september 2015 om 10.30 uur precies door Jeroen Alexander Scheper geboren op 2 november 1978 te Hengelo, Overijssel Promotoren: prof. dr. H. Siepel prof. dr. J.H.J. Schaminée Copromotor: prof. dr. ir. D. Kleijn (WUR) Manuscriptcommissie: prof. dr. J.C.J.M. de Kroon prof. dr. G.R. de Snoo (UL) prof. dr. M.F. Wallis de Vries (WUR) Contents Chapter 1 General introduction 7 Chapter 2 Museum specimens reveal loss of pollen host plants as key 17 factor driving wild bee decline in The Netherlands Chapter 3 Does conservation on farmland contribute to halting the 37 biodiversity decline? Chapter 4 Environmental factors driving the effectiveness of European 55 agri- environmental measures in mitigating pollinator loss – a meta-analysis Chapter 5 Local and landscape-level floral resources explain effects of 101 wildflower strips on wild bees across four European countries Chapter 6 Do wildflower strips enhance populations of trap-nesting bees? 127 Chapter 7 General discussion 147 Summary 159 Samenvatting 163 Dankwoord 169 List of publications 173 Curriculum vitae 175 CHAPTER 1 General introduction 7 Wild bees and ecosystem service delivery Bees (Hymenoptera: Apoidea: Apiformes) comprise a large group of flower-visiting insects, with ca. 20,000 species occurring worldwide (Michener 2007) and ca. 2,000 species occurring in Europe (Nieto et al. 2014). Flower-visiting insects such as wild bees play a vital functional role in the pollination of both wild plants and crops. The large majority of wild plants are pollinated by insects (Ollerton et al. 2011) and insect pollinators thereby form an essential component in the maintenance of biodiverse plant communities and ecosystem functioning. Furthermore, about 75% of the main global food crop species rely on insect-mediated pollination (Klein et al. 2007). Although comprising only 35% of global food production volume (Klein et al. 2007), insect-pollinated crops provide the majority of many essential vitamins and micronutrients in human nutrition (Eilers et al. 2011). The extent to which these crops depend on pollination by insects varies from essential in dioecious (e.g. most kiwi varieties) or self-infertile monoecious crops (e.g. most apple varieties), to beneficial in self- fertile hermaphroditic crops (e.g. strawberry), with insect-pollination enhancing fruit set, seed set, fruit quality and commercial value (Bommarco et al. 2012b; Garibaldi et al. 2013; Garratt et al. 2014; Klatt et al. 2014). The area of insect-pollinated crops has increased over the last decades, both at a global and a European scale (Aizen et al. 2008; Breeze et al. 2014). In Europe, 84% of crop species grown for human consumption, livestock consumption, green manure or essential oils are pollinated by insects (Williams 1994), currently representing 12% of the total EU cropland area (Schulp et al. 2014). With the annual economic value of pollination (i.e. the part of the crop yield that can be attributed to pollination) of European food crops estimated at €22 billion (Gallai et al. 2009), pollination by flower-visiting insects is a pre-eminent ecosystem service that is of particular economic importance in agricultural landscapes. A wide variety of insects, such as flies, beetles, wasps and butterflies, may contribute to the pollination of wild plants and crops, but bees generally provide by far the largest contribution (Herrera 1987; Albrecht et al. 2007; Jauker et al. 2012; Garibaldi et al. 2013; King et al. 2013). Bees fully depend on floral resources such as pollen and nectar for food provisioning in both their larval and adult life stages. Because of their dependence on floral resources, their foraging behaviour and their morphological adaptations to efficiently collect and transport pollen, bees are considered superior pollinators compared to other flower- visiting insects (Free 1993). The managed honeybee (Apis mellifera) has long been regarded as the most important crop pollinator (Klein et al. 2007). Managed honeybee colonies provide large numbers of worker bees and can easily be moved to flowering crops to provide abundant pollinators. However, the role of wild bee species has thus far been underestimated (Breeze et al. 2011). Recent evidence shows that for most crops wild pollinators are more effective pollinators than honeybees and provide the majority of pollination services, suggesting that honeybees can supplement, but not replace the pollination services of wild pollinators (Garibaldi et al. 2013). Even for crops predominantly dependent on honeybees, wild pollinators can play an important indirect role by enhancing the pollination efficiency of honeybees through synergetic effects (Greenleaf & Kremen 2006; Brittain et al. 2013). In view of increasing concern about declining numbers of honey bee colonies driven by colony losses and declining number of beekeepers (Potts et al. 2010b; Van der Zee et al. 2012), wild bees are expected to become increasingly important for pollination of crops in Europe (Breeze et al. 2014). Diverse wild bee communities improve the temporal stability of pollination service delivery and can provide insurance of pollination services under environmental change (Garibaldi et al. 2011; Bartomeus et al. 2013). However, while pollination service supply of honeybees depends on beekeepers (Potts et al. 2010b), pollination by wild bees depends on the availability of foraging and nesting sites in the landscapes surrounding the crops (Schulp et al. 2014). Insect-pollinated crops can be 8 attractive and highly rewarding sources of pollen and nectar for wild bees in agricultural landscapes (Westphal et al. 2003; Holzschuh et al. 2013). However, these crops flower for only a short period of time and the crop monocultures provide an unbalanced food supply for bees (Holzschuh et al. 2013; Eckhardt et al. 2014). Furthermore, frequent disturbance by agricultural practices (e.g. tillage, pesticide application) generally makes crops unsuitable permanent habitats for bees, especially if intensively managed (Holzschuh et al. 2007). To persist in agricultural landscapes, wild bees therefore depend on semi-natural habitats such as forest edges and semi-natural grasslands that provide a more diverse and continuous supply of floral resources and nesting, mating and overwintering sites. Such semi-natural habitats support abundant and diverse bee communities and can act as source habitats for wild pollinators in the agricultural matrix (Tscharntke et al. 2005; Öckinger & Smith 2007; Kohler et al. 2008). Consequently, pollinator richness and abundance in insect-pollinated crops is higher in landscapes containing more high-quality semi-natural habitats (Kennedy et al. 2013; Shackelford et al. 2013), and visitation rates, stability of pollination services and crop yields increase with decreasing distance to semi-natural source habitats (Ricketts et al. 2008; Garibaldi et al. 2011). Bee declines in agricultural landscapes While the importance of wild bees as ecosystem service providers is increasingly becoming acknowledged, evidence is mounting that many wild bee species have declined in Europe over the last decades (Biesmeijer et al. 2006; Kosior et al. 2007; Patiny et al. 2009; IUCN 2014). The bee communities of contemporary intensively farmed landscapes have been strongly impoverished (Kleijn et al. 2001; Bommarco et al. 2012a; Dupont et al. 2011). Many previously widespread bee species in agricultural landscapes are now only found in nature reserves (Kohler et al. 2008) or (sub)urban refugia (Samnegard et al. 2011). It appears that in northwest Europe the rate of decline of wild bee richness has slowed down in recent years (Carvalheiro et al. 2013). However, as bee communities have become more homogenized during earlier periods of decline (Carvalheiro et al. 2013), the reduced rate of species richness decline probably reflects that bee communities are currently dominated by a limited number of more resilient bee species that remained common. Climate change, invasive species and spread of pathogens have been identified as potential factors associated with pollinator declines, but land use change and agricultural intensification