Skip to main content

Wild bees respond complementarily to ‘high-quality’ perennial and annual habitats of organic farms in a complex landscape

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 habitats, 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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Amiet F (1994) Rote Listen der gefährdeten Tierarten in der Schweiz. Edt P Duelli, pp 38–44 BUWAL

  2. Aviron S, Nitsch H, Jeanneret P, Buholzer S, Luka H, Pfiffner L, Pozzi S, Schüpbach B, Walter T, Herzog F (2009) Ecological cross compliance promotes farmland biodiversity in Switzerland. Front Ecol Environ 7:247–252

    Article  Google Scholar 

  3. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7. http://CRAN.R-project.org/package=lme4

  4. Biesmeijer JC, Roberts SP, Reemer M, Ohlemuller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354

    CAS  Article  Google Scholar 

  5. Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York, p 306

    Book  Google Scholar 

  6. Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615

    CAS  Article  Google Scholar 

  7. Carrié R, Andrieu E, Cunningham SA, Lentini PE, Loreau M, Ouin A (2017) Relationships among ecological traits of wild bee communities along gradients of habitat amount and fragmentation. Ecography 40(1):85–97

    Article  Google Scholar 

  8. Clough YA, Holzschuh A, Gabriel D, Purtauf T, Kleijn D, Kruess A, Deweter IS, Tscharntke T (2007) Alpha and beta diversity of arthropods and plans in organically and conventionally managed wheat fields. J Appl Ecol 44:804–812

    Article  Google Scholar 

  9. Clough Y, Ekroos J, Báldi A, Batáry P, Bommarco R, Gross N, Holzschuh A, Hopfenmüller S, Knop E, Kuussaari M (2014) Density of insect-pollinated grassland plants decreases with increasing surrounding land-use intensity. Ecol Lett 17:1168–1177

    Article  Google Scholar 

  10. De Palma A, Kuhlmann M, Roberts SP, Potts SG, Börger L, Hudson LN, Purvis A (2015) Ecological traits affect the sensitivity of bees to land-use pressures in European agricultural landscapes. J Appl Ecol 52(6):1567–1577

    Article  Google Scholar 

  11. Forrest JRK, Thorp RW, Kremen C, Williams NM (2015) Contrasting patterns in species and functional-trait diversity of bees in an agricultural landscape. J Appl Ecol 52:706–715

    Article  Google Scholar 

  12. Garibaldi LA, Steffan-Dewenter I, Kremen D, Morales JM, Bommarco R, Cunningham SA, Carvalheiro LG, Chacoff NP, Dudenhoeffer JH, Greenleaf SS (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072

    Article  Google Scholar 

  13. Garibaldi LA, Carvalheiro LG, Leonhardt SD, Aizen MA, Blaauw BR, Isaacs R. Kuhlmann M, Kleijn M, Klein AM, Kremen C, Morandin L, Scheper J, Winfree R (2014) From research to action: enhancing crop yield through wild pollinators. Front Ecol Environ 12:439–447

    Article  Google Scholar 

  14. Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71(5):757–764

    Article  Google Scholar 

  15. Gelman A, Su Y (2014) Arm: data analysis using regression and multilevel/hierarchical models R package version 17-03 2014. Cambridge University Press, New York

    Google Scholar 

  16. Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severly affects individual- and colony-level traits in bees. Nature 491:105–109

    CAS  Article  Google Scholar 

  17. Giraudoux P (2014) pgirmess: Data analysis in ecology. https://cran.r-project.org/web/packages/pgirmess/index.html

  18. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957

    Article  Google Scholar 

  19. Holzschuh A, Steffan-Dewenter I, Kleijn D, Tscharntke T (2007) Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context. J Appl Ecol 44:41–49

    Article  Google Scholar 

  20. Holzschuh A, Steffan-Dewenter I, Tscharntke T (2008) Agricultural landscapes with organic crop support higher pollinator diversity. Oikos 117:354–361

    Article  Google Scholar 

  21. Hothorn T, Bretz F, Heiberger RM, Schuetzmeister A (2015) multcomp: Simultaneous inference in general parametric model. https://cran.r-project.org/web/packages/multcomp/index.html

  22. Jönsson AM, Ekroos J, Dänhardt J, Andersson GKS, Olsson O, Smith HG (2015) Sown flower strips in southern Sweden increase abundances of wild bees and hoverflies in the wider landscape. Biol Conserv 184:51–58

    Article  Google Scholar 

  23. Kleijn AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313

    Article  Google Scholar 

  24. Knight ME, Osborne JL, Sanderson RA, Hale RJ, Martin AP, Goulson D (2009) Bumblebee nest density and the scale of available forage in arable landscapes. Insect Conserv Divers 2:116–124

    Article  Google Scholar 

  25. Kovács-Hostyánszki A, Espíndola A, Vanbergen AJ, Settele J, Kremen C, Dicks LV (2017) Ecological intensification to mitigate impacts of conventional intensive land use on pollinators and pollination. Ecol Lett 20:673–689

    Article  Google Scholar 

  26. Kremen C, Gonigle LKM (2015) Small-scale restoration in intensive agricultural landscapes supports more specialized and less mobile pollinator species. J Appl Ecol 52(3):602–610

    Article  Google Scholar 

  27. Le Féon V, Burel F, Chifflet R, Henry M, Ricroch A, Vaissière BE, Baudry J (2013) Solitary bee abundance and species richness in dynamic agricultural landscapes. Agric Ecosyst Environ 166:94–101

    Article  Google Scholar 

  28. Michener CD (2007) The bees of the world, 2nd edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  29. Müller A, Diener S, Schnyder S, Stutz K, Sedivy C, Dorn S (2006) Quantitative pollen requirements of solitary bees: implications for bee conservation and the evolution of bee-flower relationships. Biol Conserv 130:604–615

    Article  Google Scholar 

  30. Oertli S, Müller A, Dorn S (2005) Ecological and seasonal patterns of diversity in a species-rich bee assemblage (Hymenoptera: Apoidea: Apiformes). Eur J Entomol 102:53–63

    Article  Google Scholar 

  31. Pe’er G, Dicks LV, Visconti P, Arlettaz R, Báldi A, Benton TG, Collins S, Dieterich M, Gregory RD, Hartig F, Henle K, Hobson PR, Kleijn D, Neumann RK, Robijns T, Schmidt J, Shawartz A, Sutherland WJ, Turbé A, Wulf F, Scott AV (2014) EU agricultural reform fails on biodiversity. Science 344:1090–1092

    Article  Google Scholar 

  32. Potts SG, Vulliamy B, Dafni A, Ne´man G, Willmer P (2003) Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84(10):2628–2642

    Article  Google Scholar 

  33. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  Google Scholar 

  34. Power EF, Stout JC (2011) Organic dairy farming: impacts on insect-flower interaction networks and pollination. J Appl Ecol 48:561–569

    Article  Google Scholar 

  35. R Development Core Team (2014) R: A language and environment for statistical computing. R Foundationfor Statistical Computing, Vienna

    Google Scholar 

  36. Rader R, Bartomeus I, Tylianakis JM, Laliberté E (2014) The winners and losers of land use intensification: pollinator community disassembly is non-random and alters functional diversity. Div Distrib 20:908–917

    Article  Google Scholar 

  37. Roulston TH, Goodell K (2011) The role of resources and risks in regulating wild bee populations. Ann Rev Entomol 56:293–312

    CAS  Article  Google Scholar 

  38. Sardiñas HS, Kremen C (2014) Evaluating nesting microhabitat for ground-nesting bees using emergence traps. Basic Appl Ecol 15(2):161–168

    Article  Google Scholar 

  39. Sardiñas HS, Kremen C (2015) Pollination services from field-scale agricultural diversification may be context-dependent. Agric Ecosyst Environ 207:17–25

    Article  Google Scholar 

  40. Schwarz M, Gusenleitner F, Westrich P, Dathe HH (1996) Katalog der Bienen Österreich, Deutschlands und der Schweiz (Hymenoptera, Apidae) Entomofauna Supplement 8 p 398 Linz

  41. Sokal RR, Rohlf FJ (1995) Biometry. WH Freeman, San Francisco CA

  42. Steffan-Dewenter I, Tscharntke T (2001) Succession of bee communities on fallows. Ecography 24(1):83–93

    Article  Google Scholar 

  43. Strohm E, Bordon-Hauser A (2003) Advantages and disadvantages of large colony size in a halictid bee: the queen’s perspective. Behav Ecol 14(4):546–553

    Article  Google Scholar 

  44. Sutherland WJ (2006) Ecological census techniques: a handbook, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  45. Swiss Confederation (2010) Verordnung über die biologische Landwirtschaft und die Kennzeichnung biologisch produzierter Erzeugnisse und Lebensmittel (Bio-Verordnung)

  46. Swiss Confederation (2013) Verordnung vom 23 Oktober 2013 über die Direktzahlungen an die Landwirtschaft Bundesrat Bern Switzerland

  47. Westphal C, Bommarco R, Carré G, Lamborn E, Morison N, Petanidou T, Potts SG, Roberts SPM, Szentgyörgyi H, Tscheulin T (2008) Measuring bee diversity in different European habitats and biogeographical regions. Ecol Monogr 78:653–671

    Article  Google Scholar 

  48. Westrich P (1990) Die Wildbienen Baden-Württembergs 2 Bände Suttgart: Eugen Ulmer Verlag

  49. Whitehorn PR, O’Connor S, Wäckers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumblebee colony growth and queen production. Science 336:351–352

    CAS  Article  Google Scholar 

  50. Winfree R, Aguilar R, Vazquez DP, LeBuhn G, Aizen MA (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076

    Article  Google Scholar 

  51. Wood TJ, Holland JM, Goulson D (2016) Diet characterisation of solitary bees on farmland: dietary specialisation predicts rarity. Biodivers Conserv 25:2655–2671

    Article  Google Scholar 

  52. Zurbuchen A, Müller A (2012) Wildbienenschutz – von der Wissenschaft zur Praxis Bristol-Stiftung Zürich Haupt-Verlag Bern

  53. Zurbuchen A, Landert L, Klaiber J, Müller A, Hein S, Dorn S (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv 143(3):669–676

    Article  Google Scholar 

  54. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgements

We thank Dreiklang Foundation, Vontobel Foundation, Temperatio Foundation and Oekoenergie Fonds (IWB) for their financial support. We would like to thank Fabian Cahenzli for fruitful comments, Simon Moakes for improving the English style and all participating farmers for their support and access to their fields and two anonymous reviewers for their useful and constructive comments.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lukas Pfiffner.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 946 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pfiffner, L., Ostermaier, M., Stoeckli, S. et al. Wild bees respond complementarily to ‘high-quality’ perennial and annual habitats of organic farms in a complex landscape. J Insect Conserv 22, 551–562 (2018). https://doi.org/10.1007/s10841-018-0084-6

Download citation

Keywords

  • Wild bees
  • Agri-environmental scheme
  • Biodiversity
  • Semi-natural habitats
  • Low-input habitats
  • Sustainable agriculture