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Downloading Material Is Agreeing to Abide by the Terms of the Repository Licence Cronfa - Swansea University Open Access Repository _____________________________________________________________ This is an author produced version of a paper published in : Journal of Applied Ecology Cronfa URL for this paper: http://cronfa.swan.ac.uk/Record/cronfa22329 _____________________________________________________________ Paper: Borger, L. (in press). Ecological traits affect the sensitivity of bees to land-use pressures in European agricultural landscapes. Journal of Applied Ecology _____________________________________________________________ This article is brought to you by Swansea University. Any person downloading material is agreeing to abide by the terms of the repository licence. Authors are personally responsible for adhering to publisher restrictions or conditions. When uploading content they are required to comply with their publisher agreement and the SHERPA RoMEO database to judge whether or not it is copyright safe to add this version of the paper to this repository. http://www.swansea.ac.uk/iss/researchsupport/cronfa-support/ Journal of Applied Ecology Ecological traits affect the sensitivity of bees to land -use pressures in European agricultural landscapes Journal:For Journal Peer of Applied Ecology Review Manuscript ID: JAPPL-2015-00033.R2 Manuscript Type: Standard Paper Date Submitted by the Author: 03-Jun-2015 Complete List of Authors: De Palma, Adriana; Imperial College London, Department of Life Sciences; Natural History Museum, Department of Life Sciences Kuhlmann, Michael; Natural History Museum, Department of Life Sciences Roberts, Stuart; The University of Reading, Centre for Agri-Environmental Research, School of Agriculture, Policy and Development Potts, Simon; The University of Reading, Centre for Agri-Environmental Research, School of Agriculture, Policy and Development Börger, Luca; Swansea University, Department of Biosciences, College of Science Hudson, Lawrence; Natural History Museum, Department of Life Sciences Lysenko, Igor; Imperial College London, Department of Life Sciences Newbold, Tim; United Nations Environment Programme World Conservation Monitoring Centre, Purvis, Andy; Natural History Museum, Department of Life Sciences; Imperial College London, Department of Life Sciences life-history traits, human impacts, ecosystem services, biodiversity, Key-words: pollinators, land-use change, land-use intensification Page 1 of 71 Journal of Applied Ecology Ecological traits affect the sensitivity of bees to land-use pressures in European agricultural landscapes Adriana De Palma1,2, Michael Kuhlmann2, Stuart P.M. Roberts3, Simon G. Potts3, Luca BFor¨orger4, Lawrence Peer N. Hudson Review2, Igor Lysenko1, Tim Newbold5 and Andy Purvis2,1 1Department of Life Sciences, Imperial College London, Silwood Park, SL5 7PY, UK 2Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK. 3Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, The University of Reading, Reading RG6 6AR, UK. 4Department of Biosciences, College of Science, Swansea University, Singleton Park, Swansea SA2 8PP, UK. 5United Nations Environment Programme World Conservation Monitoring Centre, 219 Huntington Road, Cambridge CB3 0DL, UK. Running title: European bee responses to land-use pressures Word Count: Summary: 282 words; main text: 3880 words; acknowledgements: 120 words; references: 1615 words; tables and figure legends: 1077 Number of tables: 4 Number of Figures: 4 Journal of Applied Ecology Page 2 of 71 Number of references: 65 Corresponding Author: Adriana De Palma, [email protected], Department of Life Sciences, Impe- rial College London, Silwood Park, SL5 7PY, UK. For Peer Review Page 3 of 71 Journal of Applied Ecology 1 Summary 2 1. Bees are a functionally important and economically valuable group, but are threatened by 3 land-use conversion and intensification. Such pressures are not expected to affect all species 4 identically; rather, they are likely to be mediated by the species’ ecological traits. 5 2. Understanding which types of species are most vulnerable under which land uses is an 6 important step towards effective conservation planning. 7 3. We collatedFor occurrence andPeer abundance dataReview for 257 bee species at 1,584 European sites 8 from surveys reported in 30 published papers (70,056 records), and combined them with 9 species-level ecological trait data. We used mixed-effects models to assess the importance 10 of land use (land-use class, agricultural use-intensity and a remotely-sensed measure of 11 vegetation), traits, and trait × land use interactions, in explaining species occurrence and 12 abundance. 13 4. Species’ sensitivity to land use was most strongly influenced by foraging range and flight 14 season, but also by niche breadth, phenology and reproductive strategy, with effects that 15 differed among cropland, pastoral and urban habitats. 16 5. Synthesis and applications. Rather than targeting particular species or settings, conser- 17 vation actions may be more effective if focused on mitigating situations where species’ 18 traits strongly and negatively interact with land-use pressures. We find evidence that low- 19 intensity agriculture can maintain relatively diverse bee communities; in more intensive 20 settings, added floral resources may be beneficial, but will require careful placement with 21 respect to foraging ranges of smaller bee species. Protection of semi-natural habitats is es- 22 sential, however; in particular, conversion to urban environments could have severe effects 23 on bee diversity and pollination services. Our results highlight the importance of exploring 24 how ecological traits mediate species responses to human impacts, but further research is 25 needed to enhance the predictive ability of such analyses. Journal of Applied Ecology Page 4 of 71 26 Keywords 27 Life-history traits; human impacts; ecosystem services; biodiversity, pollinators, land-use change, 28 land-use intensification. For Peer Review Page 5 of 71 Journal of Applied Ecology 29 Introduction 30 Bees are key providers of pollination services, which are vital for food security and the persistence 31 of many wild plants (Klein et al. 2007; Ollerton, Winfree & Tarrant 2011). However, many 32 bee species are threatened by changing and intensifying land use (Ollerton et al. 2014; Potts 33 et al. 2010). 34 Land-use change, such as conversion from semi-natural habitats to human-dominated land- 35 uses, can greatly impact bee communities. Urbanization, agricultural expansion and abandon- 36 ment are ongoingFor drivers of land-use Peer change in Europe Review (Verburg et al. 2006), which can affect bee 37 diversity through reduced floral and nesting resources (Forrest et al. 2015; Hernandez, Frankie & 38 Thorp 2009). Semi-natural habitats are prime targets for land conversion (Verburg et al. 2006). 39 Such habitat loss can affect pollination of crops as well as of wild flowers: as central place foragers, 40 bees often forage up to a few kilometres away from their nests (Greenleaf et al. 2007) so semi- 41 natural habitat can provide spill-over of pollination services to nearby cropland and vice-versa 42 (Blitzer et al. 2012). 43 Agricultural intensification—through decreased crop diversity and increased external inputs— 44 is another major pressure, which can impact bees directly by increasing mortality and indirectly 45 by decreasing resource availability (Potts et al. 2010; Roulston & Goodell 2011). For instance, 46 neonicotinoid pesticides restrict colony growth and queen production in bumblebees, and limit 47 foraging success and survival of honeybees (Henry et al. 2012; Whitehorn et al. 2012). Nitrogen 48 fertilizer and herbicides can affect bees indirectly by reducing the diversity of plants (Kleijn 49 et al. 2009) and thus foraging resources (Roulston & Goodell 2011). Reductions in non-crop 50 habitat as management intensifies can reduce the availability of nesting sites, while increased 51 tillage in cropland disturbs the nesting sites of some species (Shuler, Roulston & Farris 2005). 52 These pressures are unlikely to affect all species identically, but are expected to be mediated 53 by species’ traits (Murray et al. 2009; Roulston & Goodell 2011). In general, species with 54 narrower niches—in terms of space, time, phenotype, or interspecific interactions—are predicted 55 to be more sensitive than generalists (Den Boer 1968; Kassen 2002). Bee species’ traits may 56 specifically influence vulnerability to land use; for instance, larger foraging ranges facilitate for- 57 aging in fragmented landscapes, but may increase the likelihood of contact with pesticides and Journal of Applied Ecology Page 6 of 71 58 indicate greater resource needs. Others traits can influence susceptibility to demographic stress 59 and stochastic events; for example, a higher reproductive capacity may buffer species against 60 disturbances, but may indicate greater resource requirements. 61 Identifying traits that render species vulnerable to human impacts can help inform and guide 62 effective conservation priorities. Most previous attempts to identify ecological correlates of bee 63 vulnerability to human impacts have focused on a relatively small number of sites and threats, or 64 on museum collections rather than ecological survey data (e.g. Bartomeus et al. 2013a; V´azquez & 65 Simberloff 2002). One exception is Williams et al’s (2010) global multi-species analysis, which 66 found that someFor traits correlated Peer with vulnerability Review to multiple threats: for instance, above-
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