Landscape Ecology

, Volume 29, Issue 3, pp 425–435 | Cite as

Early mass-flowering crops mitigate pollinator dilution in late-flowering crops

  • Verena Riedinger
  • Marion Renner
  • Maj Rundlöf
  • Ingolf Steffan-Dewenter
  • Andrea Holzschuh
Research Article


Previous studies focused mainly on the provision of ecosystem services by species movements between semi-natural and managed habitats, whereas data on spillover effects between two managed habitats or between habitats that provide target resources in non-overlapping time periods are lacking. We studied densities of three pollinator groups on sunflower fields as a late mass-flowering crop in 16 landscapes that differed in the relative cover of oil-seed rape as an early mass-flowering crop, in the relative cover of sunflowers and in the relative cover of semi-natural habitats. Our aim was to evaluate dynamics between two crops with non-overlapping flowering periods. Densities of bumble bees in late-flowering sunflower fields were enhanced by early-flowering oil-seed rape. Highest bumble bee densities in the late-flowering crop were reached in landscapes that combined high relative covers of oil-seed rape and semi-natural habitats. Further, low relative covers of oil-seed rape in spring led to decreased bumble bee densities in late-flowering sunflower fields in landscapes with high relative covers of sunflower fields (dilution effect), whereas in landscapes with high relative covers of oil-seed rape, no dilution of bumble bees was found. Thus, our results indicate that early mass-flowering crops can mitigate pollinator dilution in crops flowering later in the season. We conclude that the management of landscape-scale patterns of early and late mass-flowering crops together with semi-natural habitats could be used to ensure crop pollination services. Similar processes could also apply for other species groups and may be an important, but so far disregarded, determinant of population densities in agroecosystems.


Apis mellifera Bombus Germany Oil-seed rape Spillover Sunflower Syrphids 



We thank the “Bayerisches Staatsministerium für Ernährung, Landwirtschaft und Forsten” for providing us with the landscape data, Ante Vujic for identifying the hoverflies and the land owners for the provision of the study fields. The study was funded by the European Commission under the 7th Framework Programme for Research and Technological Development. Grant agreement number: 244090—STEP—CP—FP.

Supplementary material

10980_2013_9973_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 19 kb)


  1. Aslan MM, Yavuksuz C (2010) Effect of honey bee (Apis mellifera L.) and bumblebee (Bombus terrestris L.) pollinators on yield and yield factors in sunflower (Helianthus annuus L.) production areas. J Anim Vet Adv 9:332–335Google Scholar
  2. Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol Evol 18:182–188CrossRefGoogle Scholar
  3. Blitzer E, Dormann CF, Holzschuh A, Klein AM, Rand TA, Tscharntke T (2012) Spillover of functionally important organisms between managed and natural habitats. Agric Ecosyst Environ 146:34–43CrossRefGoogle Scholar
  4. Blüthgen N, Klein A-M (2011) Functional complementarity and specialisation: the role of biodiversity in plant–pollinator interactions. Basic Appl Ecol 12:282–291CrossRefGoogle Scholar
  5. Bommarco R, Marini L, Vaissière BE (2012) Insect pollination enhances seed yield, quality, and market value in oil-seed rape. Oecologia 169:1025–1032PubMedCrossRefGoogle Scholar
  6. Carvalheiro LG, Veldtman R, Shenkute AG, Tesfay GB, Pirk CW, Donaldson JS, Nicolson SW (2011) Natural and within-farmland biodiversity enhances crop productivity. Ecol Lett 14:251–259PubMedCrossRefGoogle Scholar
  7. Crawley MJ (2007) The R book. John Wiley & Sons, LondonCrossRefGoogle Scholar
  8. Diekötter T, Kadoya T, Peter F, Wolters V, Jauker F (2010) Oil-seed rape crops distort plant-pollinator interactions. J Appl Ecol 47:209–214CrossRefGoogle Scholar
  9. Ekroos J, Rundlöf M, Smith HG (2013) Trait-dependent responses of flower-visiting insects to distance to semi-natural grasslands and landscape heterogeneity. Landscape Ecol 28:1283–1292CrossRefGoogle Scholar
  10. European Commission (2011) Eurostat-statistics explained: agricultural products. Accessed 18 Dec 2013
  11. Fahrig L, Baudry J, Brotons L, Burel FG, Crist TO, Fuller RJ, Sirami C, Siriwardena GM, Martin JL (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112PubMedCrossRefGoogle Scholar
  12. Gallai N, Salles J-M, Settele J, Vaissière B (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821CrossRefGoogle Scholar
  13. Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Carvalheiro LG, Chacoff NP, Dudenhöffer JH, Greenleaf SS, Holzschuh A, Isaacs R, Krewenka K, Mandelik Y, Mayfield MM, Morandin LA, Potts SG, Ricketts TH, Szentgyörgyi H, Viana BF, Westphal C, Winfree R, Klein AM (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072PubMedCrossRefGoogle Scholar
  14. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596PubMedCrossRefGoogle Scholar
  15. Haenke S, Scheid B, Schaefer M, Tscharntke T, Thies C (2009) Increasing syrphid fly diversity and density in sown flower strips within simple vs. complex landscapes. J Appl Ecol 46:1106–1114CrossRefGoogle Scholar
  16. Hanley ME, Franco M, Dean CE, Franklin EL, Harris HR, Haynes AG, Rapson SR, Rowse G, Thomas KC, Waterhouse BR, Knight ME (2011) Increased bumblebee abundance along the margins of a mass flowering crop: evidence for pollinator spill-over. Oikos 120:1618–1624CrossRefGoogle Scholar
  17. Herrmann F, Westphal C, Moritz RFA, Steffan-Dewenter I (2007) Genetic diversity and mass resources promote colony size and forager densities of a social bee (Bombus pascuorum) in agricultural landscapes. Mol Ecol 16:1167–1178PubMedCrossRefGoogle Scholar
  18. Hickman J, Wratten S (1996) Use of Phacelia tanacetifolia strips enhance biological control of aphids by hoverfly larvae in cereal fields. J Econ Entomol 89:832–840Google Scholar
  19. Holzschuh A, Dormann CF, Tscharntke T, Steffan-Dewenter I (2011) Expansion of mass-flowering crops leads to transient pollinator dilution and reduced wild plant pollination. Proc Biol Sci/R Soc 278:3444–3451CrossRefGoogle Scholar
  20. Holzschuh A, Dormann CF, Tscharntke T, Steffan-Dewenter I (2012) Mass-flowering crops enhance wild bee abundance. Oecologia 172:477–484PubMedCentralPubMedCrossRefGoogle Scholar
  21. Jauker F, Diekötter T, Schwarzbach 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 Ecol 24:547–555CrossRefGoogle Scholar
  22. Jauker F, Peter F, Wolters V, Diekötter T (2012) Early reproductive benefits of mass-flowering crops to the solitary bee Osmia rufa outbalance post-flowering disadvantages. Basic Appl Ecol 13:268–276CrossRefGoogle Scholar
  23. Kleijn D, Van Langevelde F (2006) Interacting effects of landscape context and habitat quality on flower visiting insects in agricultural landscapes. Basic Appl Ecol 7:201–214CrossRefGoogle Scholar
  24. Klein A-M, Vaissie BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc Biol Sci/R Soc 274:303–313CrossRefGoogle Scholar
  25. Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. PNAS 99:16812–16816PubMedCrossRefGoogle Scholar
  26. Le Féon V, Burel F, Chifflet R, Henry M, Ricroch AE, Vaissiere BE, Baudry J (2013) Solitary bee abundance and species richness in dynamic agricultural landscapes. Agric Ecosyst Environ 166:94–101CrossRefGoogle Scholar
  27. Martin EA, Reineking B, Seo B, Steffan-Dewenter I (2013) Natural enemy interactions constrain pest control in complex agricultural landscapes. PNAS 110:5534–5539PubMedCrossRefGoogle Scholar
  28. Meyer B, Jauker F, Steffan-Dewenter I (2009) Contrasting resource-dependent responses of hoverfly richness and density to landscape structure. Basic Appl Ecol 10:178–186CrossRefGoogle Scholar
  29. Morandin LA, Winston ML (2006) Pollinators provide economic incentive to preserve natural land in agroecosystems. Agric Ecosyst Environ 116:289–292CrossRefGoogle Scholar
  30. Mudri-Stojnic S, Andric A, Józan Z, Vujic A (2012) Pollinator diversity (Hymenoptera and Diptera) in semi-natural habitats in Serbia during summer. Arch Biol Sci 64:777–786CrossRefGoogle Scholar
  31. Öckinger E, Smith HG (2007) Semi-natural grasslands as population sources for pollinating insects in agricultural landscapes. J Appl Ecol 44:50–59CrossRefGoogle Scholar
  32. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326CrossRefGoogle 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 25:345–353PubMedCrossRefGoogle Scholar
  34. R Development Core Team (2012) R: a language and environment for statistical computing. Foundation for Statistical Computing, ViennaGoogle Scholar
  35. Rand TA, Tylianakis JM, Tscharntke T (2006) Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol Lett 9:603–614PubMedCrossRefGoogle Scholar
  36. Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng’ A, Potts SG, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515PubMedCrossRefGoogle Scholar
  37. Rundlöf M, Nilsson H, Smith HG (2008) Interacting effects of farming practice and landscape context on bumble bees. Biol Conserv 141:417–426CrossRefGoogle Scholar
  38. Steffan-Dewenter I, Münzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432CrossRefGoogle Scholar
  39. Tenhumberg B, Poehling H (1995) Syrphids as natural enemies of cereal aphids in Germany: aspects of their biology and efficacy in different years and regions. Agric Ecosyst Environ 52:39–43CrossRefGoogle Scholar
  40. Thies C, Tscharntke T (1999) Landscape structure and biological control in agroecosystems. Science 285:893–895PubMedCrossRefGoogle Scholar
  41. Thies C, Steffan-Dewenter I, Tscharntke T (2008) Interannual landscape changes influence plant–herbivore–parasitoid interactions. Agric Ecosyst Environ 125:266–268CrossRefGoogle Scholar
  42. Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Fründ J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev 87:661–685PubMedCrossRefGoogle Scholar
  43. Veddeler D, Klein A-M, Tscharntke T (2006) Contrasting responses of bee communities to coffee flowering at different spatial scales. Oikos 112:594–601CrossRefGoogle Scholar
  44. Westphal C, Steffan-Dewenter I, Tscharntke T (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecol Lett 6:961–965CrossRefGoogle Scholar
  45. Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149:289–300PubMedCrossRefGoogle Scholar
  46. Westphal C, Steffan-Dewenter I, Tscharntke T (2009) Mass flowering oil-seed rape improves early colony growth but not sexual reproduction of bumblebees. J Appl Ecol 46:187–193CrossRefGoogle Scholar
  47. Westrich P (1996) Habitat requirements of central European bees and the problems of partial habitats. In: Matheson A, Buchmann S, O’Toole C, Westrich P, Williams IH (eds) The conservation of bees. Academic Press, London, pp 1–16Google Scholar
  48. Williams NM, Regetz J, Kremen C (2012) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049–1058PubMedCrossRefGoogle Scholar
  49. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Verena Riedinger
    • 1
  • Marion Renner
    • 1
  • Maj Rundlöf
    • 2
  • Ingolf Steffan-Dewenter
    • 1
  • Andrea Holzschuh
    • 1
  1. 1.Department of Animal Ecology and Tropical Biology, BiocentreUniversity of WürzburgWürzburgGermany
  2. 2.Department of Biology, BiodiversityLund UniversityLundSweden

Personalised recommendations