Insect pollination enhances seed yield, quality, and market value in oilseed rape

Abstract

The relationships between landscape intensification, the abundance and diversity of pollinating insects, and their contributions to crop yield, quality, and market value are poorly studied, despite observed declines in wild and domesticated pollinators. Abundance and species richness of pollinating insects were estimated in ten fields of spring oilseed rape, Brassica napus var. SW Stratos™, located along a gradient of landscape compositions ranging from simple landscapes dominated by arable land to heterogeneous landscapes with extensive cover of semi-natural habitats. In each field, we assessed the contribution of wind and insect pollination to seed yield, seed quality (individual seed weight and oil and chlorophyll contents), and market value in a block experiment with four replicates and two treatments: (1) all flowers were accessible to insects, self and wind pollination, and (2) flowers enclosed in tulle net bags (mesh: 1 × 1 mm) were accessible only to wind and self pollination. Complex landscapes enhanced the overall abundance of wild insects as well as the abundance and species richness of hoverflies. This did not translate to a higher yield, probably due to consistent pollination by honey bees across all fields. However, the pollination experiment showed that insects increased seed weight per plant by 18% and market value by 20%. Seed quality was enhanced by insect pollination, rendering heavier seeds as well as higher oil and lower chlorophyll contents, clearly showing that insect pollination is required to reach high seed yield and quality in oilseed rape. Our study demonstrates considerable and previously underestimated contributions from pollinating insects to both the yield and the market value of oilseed rape.

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References

  1. Åhman I, Lehrman A, Ekbom B (2009) Impact of herbivory and pollination on performance and competitive ability of oilseed rape transformed for pollen beetle resistance. Arthropod-Plant Interact 3:105–113

    Article  Google Scholar 

  2. Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, Cane J, Cox PA, Dalton V, Feinsinger P, Ingram M, Inouye D, Jones CE, Kennedy K, Kevan P, Koopowitz H, Medellin R, Medellin-Morales S, Nabhan GP, Pavlik B, Tepedino V, Torchio PH, Walker S (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12:8–17. doi:10.1046/j.1523-1739.1998.97154.x

    Article  Google Scholar 

  3. Biesmeijer JC, Roberts SPM, 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. doi:10.1126/science.1127863

    PubMed  Article  CAS  Google Scholar 

  4. Bommarco R, Biesmeijer JC, Meyer B, Potts SG, Pöyry J, Roberts SPM, Steffan-Dewenter I, Öckinger E (2010) Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proc R Soc Lond B 277:2075–2082. doi:10.1098/rspb.2009.2221

    Article  Google Scholar 

  5. Bommarco R, Lundin O, Smith HG, Rundlöf M (2012) Drastic historic shifts in bumble bee community composition in Sweden. Proc R Soc Lond B 279:309–315. doi:10.1098/rspb.2011.0647

    Article  Google Scholar 

  6. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, Martinson V, vanEngelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai JH, Cui LW, Hutchison SK, Simons JF, Egholm M, Pettis JS, Lipkin WI (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283–287. doi:10.1126/science.1146498

    PubMed  Article  CAS  Google Scholar 

  7. Delaplane KS, Mayer DF (2000) Crop pollination by bees. CABI, New York

  8. FAO (2008) FAOSTAT homepage. http://faostat.fao.org/

  9. Free JB (1993) Insect pollination of crops, 2nd edn. Academic, London

  10. Fries I, Stark J (1983) Measuring the importance of honeybees in rape seed production. J Apic Res 22:272–276

    Google Scholar 

  11. Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821. doi:10.1016/j.ecolecon.2008.06.014

    Article  Google Scholar 

  12. 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, Westphal C, Winfree R, Klein AM (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072. doi:10.1111/j.1461-0248.2011.01669.x

    PubMed  Article  Google Scholar 

  13. Ghazoul J (2005) Buzziness as usual? Questioning the global pollination crisis. Trends Ecol Evol 20:367–373. doi:10.1016/j.tree.2005.04.026

    PubMed  Article  Google Scholar 

  14. Greenleaf SS, Kremen C (2006) Wild bee species increase tomato production but respond differently to surrounding land use in Northern California. Biol Conserv 133:81–87. doi:10.1016/j.biocon.2006.05.025

    Article  Google Scholar 

  15. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. doi:10.1007/s00442-007-0752-9

    PubMed  Article  Google Scholar 

  16. Hayter KE, Cresswell JE (2006) The influence of pollinator abundance on the dynamics and efficiency of pollination in agricultural Brassica napus: implications for landscape-scale gene dispersal. J Appl Ecol 43:1196–1202. doi:10.1111/j.1365-2664.2006.01219.x

    Article  Google Scholar 

  17. Hendrickx F, Maelfait JP, Van Wingerden W, Schweiger O, Speelmans M, Aviron S, Augenstein I, Billeter R, Bailey D, Bukacek R, Burel F, Diekötter T, Dirksen J, Herzog F, Liira J, Roubalova M, Vandomme V, Bugter R (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J Appl Ecol 44:340–351. doi:10.1111/j.1365-2664.2006.01270.x

    Article  Google Scholar 

  18. Holland JD, Bert DG, Fahrig L (2004) Determining the spatial scale of species’ response to habitat. Bioscience 54:227–233. doi:10.1641/0006-3568(2004)054[0227:DTSSOS]2.0.CO;2

    Google Scholar 

  19. Jauker F, Wolters V (2008) Hover flies are efficient pollinators of oilseed rape. Oecologia 156:819–823. doi:10.1007/s00442-008-1034-x

    PubMed  Article  Google Scholar 

  20. Jauker F, Bondarenko B, Becker HC, Steffan-Dewenter I (2012) Pollination efficiency of wild bees and hoverflies provided to oilseed rape. Agric For Entomol 14:81–87. doi: 10.1111/j.1461-9563.2011.00541.x

  21. Kevan PG (1975) Forest application of the insecticide Fenitrothion and its effects on wild bee pollinators (Hymenoptera: Apoidea) of lowbush blueberries (Vaccinium spp.) in southern New Brunswick. Canada. Biol Conserv 7:301–309

    Article  Google Scholar 

  22. Kleijn D, Berendse F, Smit R, Gilissen N, Smit J, Brak B, Groeneveld R (2004) Ecological effectiveness of agri-environment schemes in different agricultural landscapes in the Netherlands. Conserv Biol 18:775–786. doi:10.1111/j.1523-1739.2004.00550.x

    Article  Google Scholar 

  23. Klein A-M, Vaissiére 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 Lond B 274:303–313. doi:10.1098/rspb.2006.3721

    Article  Google Scholar 

  24. Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci USA 99:16812–16816. doi:10.1073/pnas.262413599

    PubMed  Article  CAS  Google Scholar 

  25. Langridge DF, Goodman RD (1982) Honeybee pollination of oilseed rape, cultivar Midas. Aust J Exp Agr Anim Husb 22:124–126. doi:10.1071/EA9820124

    Article  Google Scholar 

  26. Lantmännen (2005) Inför skörden 2005—lantmännens inköpsvillkor skörd 2005. Svenska Lantmännen, Norrköping

    Google Scholar 

  27. Lantmäteriet (2008) National land survey of Sweden. http://www.lantmateriet.se

  28. Manning R, Wallis IR (2005) Seed yields in canola (Brassica napus cv. Karoo) depend on the distance of plants from honeybee apiaries. Austr J Exp Agr 45:1307–1313. doi:10.1071/EA02170

    Article  Google Scholar 

  29. Meyer B, Jauker F, Steffan-Dewenter I (2009) Contrasting resource-dependent responses of hoverfly richness and density to landscape structure. Basic Appl Ecol 10:178–186. doi:10.1016/j.baae.2008.01.001

    Article  Google Scholar 

  30. Morandin LA, Winston ML (2005) Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol Appl 15:871–881. doi:10.1890/03-5271

    Article  Google Scholar 

  31. Morandin LA, Winston ML (2006) Pollinators provide economic incentive to preserve natural land in agroecosystems. Agr Ecosyst Environ 116:289–292. doi:10.1016/j.agee.2006.02.012

    Article  Google Scholar 

  32. 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. doi:10.1016/j.tree.2010.01.007

    PubMed  Article  Google Scholar 

  33. Rader R, Edwards W, Westcott DA, Cunningham SA, Howlett BG (2011) Pollen transport differs among bees and flies in a human-modified landscape. Divers Distrib 17:519–529. doi:10.1111/j.1472-4642.2011.00757.x

    Article  Google Scholar 

  34. Ricketts TH, Daily GC, Ehrlich PR, Michener CD (2004) Economic value of tropical forest to coffee production. Proc Natl Acad Sci USA 101:12579–12582. doi:10.1073/pnas.0405147101

    PubMed  Article  CAS  Google Scholar 

  35. Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein A-M, Mayfield MM, Morandin LA, Ochieng A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515. doi:10.1111/j.1461-0248.2008.01157.x

    Google Scholar 

  36. Robinson RA, Sutherland WJ (2002) Post-war changes in arable farming and biodiversity in Great Britain. J Appl Ecol 39:157–176. doi:10.1046/j.1365-2664.2002.00695.x

    Article  Google Scholar 

  37. Rundlöf M, Nilsson H, Smith HG (2008) Interacting effects of farming practice and landscape context on bumblebees. Biol Conserv 141:417–426. doi:10.1016/j.biocon.2007.10.011

    Article  Google Scholar 

  38. Sabbahi R, Dd Oliveira, Marceau J (2005) Influence of honey bee (Hymenoptera: Apidae) density on the production of canola (Crucifera: Brassicacae). J Econ Entomol 98:367–372. doi:10.1603/0022-0493-98.2.367

    PubMed  Article  Google Scholar 

  39. Sabbahi R, Dd Oliviera, Marceau J (2006) Does the honeybee (Hymenoptera: Apidae) reduce the blooming period of canola? J Agronomy Crop Sci 192:233–237. doi:10.1111/j.1439-037X.2006.00206.x

    Article  Google Scholar 

  40. Sacchi CF, Price PW (1988) Pollination of the arroyo willow, Salix lasiolepis: role of insects and wind. Am J Bot 75:1387–1393. doi:10.2307/2444462

    Article  Google Scholar 

  41. Skogsmyr I, Lankinen A (2002) Sexual selection: an evolutionary force in plants? Biol Rev 77:537–562. doi:10.1017/S1464793102005973

    PubMed  Article  Google Scholar 

  42. Steffan-Dewenter I, Münzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432. doi:10.2307/3071954

    Article  Google Scholar 

  43. Thies C, Steffan-Dewenter I, Tscharntke T (2003) Effects of landscape context on herbivory and parasitism at different spatial scales. Oikos 101:18–25. doi:10.1034/j.1600-0706.2003.12567.x

    Article  Google Scholar 

  44. Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284. doi:10.1126/science.1057544

    PubMed  Article  CAS  Google Scholar 

  45. Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874. doi:10.1111/j.1461-0248.2005.00782.x

    Google Scholar 

  46. van Treuren R, Bulsma R, Ouborg JN, van Delden W (1993) The significance of genetic erosion in the process of extinction. IV. Inbreeding depression and heterosis effects caused by selfing and outcrossing in Scabiosa columbaria. Evolution 47:1669–1680. doi:10.2307/2410211

    Google Scholar 

  47. Westphal C, Bommarco R, Carré G, Lamborn E, Morison N, Petanidou T, Potts SG, Roberts SPM, Szentgyörgyi H, Tscheulin T, Vaissière BE, Woyciechowski M, Biesmeijer JC, Kunin WE, Settele J, Steffan-Dewenter I (2008) Measuring bee biodiversity in different European habitats and biogeographical regions. Ecol Mon 78:653–671. doi:10.1890/07-1292.1

    Article  Google Scholar 

  48. Willson MF (1994) Sexual selection in plants—perspectives and overview. Am Nat 144:S13–S39. doi:10.1086/285651

    Google Scholar 

  49. Wragg PD, Johnson SD (2011) Transitions from wind pollination to insect pollination in sedges: experimental evidence and functional traits. New Phytol 191:1128–1140. doi:10.1111/j.1469-8137.2011.03762.x

    PubMed  Article  Google Scholar 

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Acknowledgments

We thank Ingolf Steffan-Dewenter, Alexandra-Maria Klein, Ingemar Fries, and two anonymous reviewers for very useful comments. Stuart McMillan, Robert Wedmo, Carol Högfeldt, and Solveig Eriksson are thanked for assistance in the field, and the farmers for their helpful collaboration. We are grateful to Erik N. Sjödin and Jean-Pierre Sarthou for help with identifying bees and syrphids, respectively. The oil and chlorophyll analysis was performed by Eva Engwall at Svalöf Weibull Labs AB, and was funded by Svensk Raps AB. This research was part of the projects “ALARM—assessing large-scale environmental risks for biodiversity with tested methods” (GOCE-CT-2003-506675) and “STEP—status and trends of European pollinators” (244090) of the EU 6th and 7th Framework Programs, respectively, and the project “SAPES” funded by FORMAS.

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Correspondence to Riccardo Bommarco.

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Communicated by Jason Tylianakis.

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Bommarco, R., Marini, L. & Vaissière, B.E. Insect pollination enhances seed yield, quality, and market value in oilseed rape. Oecologia 169, 1025–1032 (2012). https://doi.org/10.1007/s00442-012-2271-6

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Keywords

  • Brassica napus
  • Crop pollination
  • Honey bee
  • Hoverflies
  • Landscape heterogeneity