Plant Ecology and Evolution 154(3): 341-350, doi: 10.5091/plecevo.2021.1884
Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes
expand article infoLina Herbertsson, Johan Ekroos, Matthias Albrecht§, Ignasi Bartomeus|, Péter Batáry, Riccardo Bommarco#, Paul Caplat, Tim Diekötter¤, Jenny M. Eikestam, Martin H. Entling«, Sunniva Farbu, Nina Farwig», Juan P. Gonzalez-Varo˄, Annika L. Hass˅, Andrea Holzschuh¦, Sebastian Hopfenmüllerˀ, Anna Jakobssonˁ, Birgit Jauker, Anikó Kovács-Hostyánszki, Wera Kleve#, William E. Kunin, Sandra A.M. Lindström#, Sarah Mullen, Erik Öckinger, Theodora Petanidou, Simon G. Potts, Eileen F. Power, Maj Rundlof, Kathrin Seibel, Virve Sõber, Annika Söderman, Ingolf Steffan-Dewenter, Jane C. Stout, Tiit Teder, Teja Tscharntke, Henrik G. Smith
‡ Centre for Environmental and Climate Science, Lund University, Lund, Sweden§ Agroscope, Agroecology and Environment, Zürich, Switzerland| Doñana Biological Station, Seville, Spain¶ Centre for Ecological Research, Institute of Ecology and Botany, Lendület Landscape and Conservation Ecology, Vácrátót, Hungary# Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden¤ Institute for Natural Resource Conservation, Department of Landscape Ecology, Kiel University, Kiel, Germany« Institute for Environmental Sciences, University Koblenz - Landau, Landau, Germany» Department of Biology, Conservation Ecology, Philipps-Universität Marburg, Marburg, Germany˄ Estación Biológica de Doñana EBD-CSIC, Department of Integrative Ecology, Sevilla, Spain˅ Functional Agrobiodiversity, University of Göttingen, Göttingen, Germany¦ University of Wuerzburg, WUerzburg, Germanyˀ Department of Animal Ecology and Tropical Biology, Biocenter, University of Würzburg, Würzburg, Germanyˁ Högskolan Väst, Trollhättan, Sweden₵ Department of Animal Ecology, Justus Liebig University Giessen, Giessen, Germanyℓ Lendület Ecosystem Services Research Group, Institute of Ecology and Botany, Centre for Ecological Research, Vácrátót, Hungary₰ University of Leeds, Leeds, United Kingdom₱ School of Natural Sciences, Trinity College Dublin, Dublin, Ireland₳ Swedish University of Agricultural Sciences, Uppsala, Sweden₴ Department of Geography, University of the Aegean, Mytilene, Greece₣ University of Reading, Reading, United Kingdom₮ Department of Biology, Lund University, Lund, Sweden₦ Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia₭ University of Würzburg, Würzburg, Germany₲ University of Tartu, Tartu, Estonia‽ Agroecology, University of Göttingen, Göttingen, Germany
Open Access

Background and aims – Agricultural intensification and loss of farmland heterogeneity have contributed to population declines of wild bees and other pollinators, which may have caused subsequent declines in insect-pollinated wild plants.

Material and methods – Using data from 37 studies on 22 pollinator-dependent wild plant species across Europe, we investigated whether flower visitation and seed set of insect-pollinated plants decline with an increasing proportion of arable land within 1 km.

Key results – Seed set increased with increasing flower visitation by bees, most of which were wild bees, but not with increasing flower visitation by other insects. Increasing proportion of arable land had a strongly variable effect on seed set and flower visitation by bees across studies.

Conclusion – Factors such as landscape configuration, local habitat quality, and temporally changing resource availability (e.g. due to mass-flowering crops or honey bee hives) could have modified the effect of arable land on pollination. While our results highlight that the persistence of wild bees is crucial to maintain plant diversity, we also show that pollen limitation due to declining bee populations in homogenized agricultural landscapes is not a universal driver causing parallel losses of bees and insect-pollinated plants.

habitat loss, landscape complexity, landscape simplification, pollination, pollinating insects, semi-natural


  • Aguilar R., Ashworth L., Galetto L. & Aizen M.A. 2006. Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecology Letters 9: 968–980.
  • Aguilar R., Cristóbal-Pérez E.J., Balvino-Olvera F.J., et al. 2019. Habitat fragmentation reduces plant progeny quality: a global synthesis. Ecology Letters 22: 1163–1173.
  • Batáry P., Kurucz K., Suarez-Rubio M. & Chamberlain D.E. 2018. Non-linearities in bird responses across urbanization gradients: a meta-analysis. Global Change Biology 24: 1046–1054.
  • Biesmeijer J.C., Roberts S.P.M., Reemer M., et al. 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313: 351–354.
  • Bilz M., Kell S.P., Maxted N. & Lansdown R.V. 2011. European Red List of Vascular Plants. Publications Office of the European Union, Luxembourg.
  • Bobbink R., Hicks K., Galloway J., et al. 2010. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications 20: 30–59.
  • Bommarco R., Lundin O., Smith H.G. & Rundlöf M. 2012. Drastic historic shifts in bumble-bee community composition in Sweden. Proceedings of the Royal Society B 279: 309–315.
  • Burd M. 1994. Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. The Botanical Review 60: 83–139.
  • Carrié R., Ekroos J. & Smith H.G. 2018. Organic farming supports spatiotemporal stability in species richness of bumblebees and butterflies. Biological Conservation 227: 48–55.
  • Carvalheiro L.G., Biesmeijer J.C., Benadi G., et al. 2014. The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility, and relatedness. Ecology Letters 17: 1389–1399.
  • Clough Y., Ekroos J., Báldi A., et al. 2014. Density of insect-pollinated grassland plants decreases with increasing surrounding land-use intensity. Ecology Letters 17: 1168–1177.
  • Cole B., Smith G. & Balzter H. 2018. Acceleration and fragmentation of CORINE land cover changes in the United Kingdom from 2006–2012 detected by Copernicus IMAGE2012 satellite data. International Journal of Applied Earth Observation and Geoinformation 73: 107–122.
  • Cussans J., Goulson D., Sanderson R., Goffe L., Darvill B. & Osborne J.L. 2010. Two bee-pollinated plant species show higher seed production when grown in gardens compared to arable farmland. PLoS ONE 5: e11753.
  • Da Encarnação Coutinho J.G., Garibaldi L.A. & Viana B.F. 2018. The influence of local and landscape scale on single response traits in bees: a meta-analysis. Agriculture, Ecosystems and Environment 256: 61–73.
  • Ekroos J., Rundlöf M. & Smith H.G. 2013. Trait-dependent responses of flower-visiting insects to distance to semi-natural grasslands and landscape heterogeneity. Landscape Ecology 28: 1283–1292.
  • Fontaine C., Dajoz I., Meriguet J. & Loreau M. 2005. Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biology 4: e1.
  • Hass A.L., Kormann U.G., Tscharntke T., et al. 2018. Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe. Proceedings of the Royal Society B 285: 20172242.
  • Hallmann A., Ssymank A., Sorg M., de Kroon H. & Jongejans E. 2021. Insect biomass decline scaled to species diversity: general patterns derived from a hoverfly community. Proceedings of the National Academy of Sciences of the United States of America 118: e2002554117.
  • Hegland S.J., Grytnes J. & Totland Ø. 2009. The relative importance of positive and negative interactions for pollinator attraction in a plant community. Ecological Research 24: 929–936.
  • Herbertsson L., Rundlöf M. & Smith H.G. 2017. The relation between oilseed rape and pollination of later flowering plants varies across plant species and landscape contexts. Basic and Applied Ecology 24: 77–85.
  • Herbertsson L., Jönsson A.M., Andersson G.K.S., et al. 2018. The impact of sown flower strips on plant reproductive success in Southern Sweden varies with landscape context. Agriculture, Ecosystems & Environment 259: 127–134.
  • Holzschuh A., Dainese M., González-Varo JP., et al. 2016. Mass-flowering crops dilute pollinator abundance in agricultural landscapes across Europe. Ecology Letters 19: 1228–1236.
  • Honová D., Hecman M., Klaudisová M., Pavlů V., Kocourková D. & Hakl J. 2007. Species composition of an alluvial meadow after 40 years of applying nitrogen, phospohorus and potassium fertilizer. Preslia 79: 245–258.
  • Hung K.L.J., Kingston J.L., Albrecht M., Holway D.A & Kohn J.R. 2018. The worldwide importance of honey bees as pollinators in natural habitats. Proceedings of the Royal Society B 285: 20172140.
  • Jauker F., Diekötter T., Schwartzbach F. & Wolters V. 2009. Pollinator dispersal in an agricultural matrix: opposing responses of wild bees and hoverflies to landscape structure and distance from main habitat. Landscape Ecology 24: 547–555.
  • Kennedy C.M., Lonsdorf E., Neel M.C., et al. 2013. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecology Letters 16: 584–599.
  • Kleijn D. & Snoeijing G.I.J. 1997. Field boundary vegetation and the effects of agrochemical drift: botanical change caused by low levels of herbicide and fertilizer. Journal of Applied Ecology 34: 1413–1425.
  • Kovács-Hostyánszki A., Haenke S., Batáry P., et al. 2013. Contrasting effects of mass-flowering crops on bee pollination of hedge plants at different spatial and temporal scales. Ecological Applications 23: 1938–1946.
  • Kuussaari M., Heliölä J., Pöyry J. & Saarinen K. 2007. Contrasting trends of butterfly species preferring semi-natural grasslands, field margins and forest edges in northern Europe. Journal of Insect Conservation 11: 351–366.
  • Magrach A., González-Varo J.P., Boiffier M., Vilà M. & Bartomeus I. 2017. Honeybee spillover reshuffles pollinator diets and affects plant reproductive success. Nature Ecology & Evolution 1: 1299–1307.
  • Magrach A., Holzschuh A., Bartomeus I., et al. 2018. Plant–pollinator networks in semi-natural grasslands are resistant to the loss of pollinators during blooming of mass-flowering crops. Ecography 41: 62–74.
  • Mallinger R.E., Gibbs J. & Gratton C. 2016. Diverse landscapes have a higher abundance and species richness of spring wild bees by providing complementary floral resources over bees’ foraging periods. Landscape Ecology 31: 1523–1535.
  • Marja R., Viik E., Mänd M., Phillips J., Klein A-M. & Batáry P. 2018. Crop rotation and agri-environment schemes determine bumblebee communities via flower resources. Journal of Applied Ecology 55: 1714–1724.
  • Martin E.A., Dainese M., Clough Y., et al. 2019. The interplay of landscape composition and configuration: new pathways to manage functional biodiversity and agroecosystem services across Europe. Ecology Letters 22: 1083–1094.
  • Mesgaran M.B., Bouhours J., Lewis M.A. & Cousens R.D. 2017. How to be a good neighbour: facilitation and competition between two co-flowering species. Journal of Theoretical Biology 422: 72–83.
  • Morales C.L. & Traveset A. 2008. Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Critical Reviews in Plant Sciences 27: 221–238.
  • Papanikolaou A.D., Kühn I., Frenzel M., et al. 2017. Wild bee and floral diversity co-vary in response to the direct and indirect impacts of land use. Ecosphere 8: e02008.
  • Persson A.S. & Smith H.G. 2013. Seasonal persistence of bumblebee populations is affected by landscape context. Agriculture, Ecosystems & Environment 165: 201–209.
  • Persson A.S., Rundlöf M., Clough Y. & Smith H.G. 2015. Bumble bees show trait-dependent vulnerability to landscape simplification. Biodiversity and Conservation 24: 3469–3489.
  • Power E.F., Jackson Z. & Stout J.C. 2016. Organic farming and landscape factors affect abundance and richness of hoverflies (Diptera, Syrphidae) in grasslands. Insect Conservation and Diversity 9: 244–253.
  • Qi M., Sun T., Xue S., Yang W., Shao D. & Martínez-López J. 2018. Competitive ability, stress tolerance and plant interactions along stress gradients. Ecology 99: 848–457.
  • R Core Team 2021. R: a language and environment for statistical computing. Version 4.1.0. R Foundation for Statistical Computing, Vienna. Available from [accessed 8 Oct. 2021].
  • Rundlöf M., Persson A.S., Smith H.G. & Bommarco R. 2014. Late-season mass-flowering red clover increases bumble bee queen and male densities. Biological Conservation 172: 138–145.
  • Scheper J., Reemer M., van Kats R., et al. 2014. Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline in The Netherlands. Proceedings of the National Academy of Sciences of the United States of America 111: 17552–17557.
  • Smith H.G., Birkhofer K., Clough Y., Ekroos J., Olsson O. & Rundlöf M. 2014. Beyond dispersal: the role of animal movement in modern agricultural landscapes. In: Hansson L.-A. & Åkesson S. (eds) Animal movement across scales. Oxford University Press, Oxford.
  • Steffan-Dewenter I., Münzenberg U. & Tscharntke T. 2001. Pollination, seed set and seed predation on a landscape scale. Proceedings of the Royal Society B 268: 1685–1690.
  • Theodose T.A. & Bowman W.D. 1997. The influence of interspecific competition on the distribution of an alpine graminoid: evidence for the importance of plant competition in an extreme environment. Oikos 79: 101–114.
  • Tuck S.L., Winqvist C., Mota F., Ahnström J., Turnbull L.A. & Bengtsson J. 2014. Land-use intensity and the effects of organic farming on biodiversity: a hierarchical meta-analysis. Journal of Applied Ecology 51: 746–755.
  • Tyler T., Herbertsson L., Olsson P.A., et al. 2018. Climate warming and land‐use changes drive broad‐scale floristic changes in Southern Sweden. Global Change Biology 24: 2607–2621.
  • Vamosi J.C., Knight T.M., Steets J.A., Mazer S.J., Burd M. & Ashman T.-L. 2006. Pollination decays in biodiversity hotspots. Proceedings of the National Academy of Sciences of the United States of America 103: 956–961.
  • Walther-Hellwig K. & Frankl R. 2000. Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., Apidae), in an agricultural landscape. Journal of Applied Entomology 124: 299–306.
  • Westphal C., Steffan-Dewenter I. & Tscharntke T. 2006. Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149: 289–300.
  • Winfree R., Aguilar R., Vázquez D.P., LeBuhn G. & Aizen M.A. 2009. A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90: 2068–2076.