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Large-scale pollination experiment demonstrates the importance of insect pollination in winter oilseed rape

  • Plant-microbe-animal interactions - Original research
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Abstract

Insect pollination, despite its potential to contribute substantially to crop production, is not an integrated part of agronomic planning. A major reason for this are knowledge gaps in the contribution of pollinators to yield, which partly result from difficulties in determining area-based estimates of yield effects from insect pollination under field conditions. We have experimentally manipulated honey bee Apis mellifera densities at 43 oilseed rape Brassica napus fields over 2 years in Scandinavia. Honey bee hives were placed in 22 fields; an additional 21 fields without large apiaries in the surrounding landscape were selected as controls. Depending on the pollination system in the parental generation, the B. napus cultivars in the crop fields are classified as either open-pollinated or first-generation hybrids, with both types being open-pollinated in the generation of plants cultivated in the fields. Three cultivars of each type were grown. We measured the activity of flower-visiting insects during flowering and estimated yields by harvesting with small combine harvesters. The addition of honey bee hives to the fields dramatically increased abundance of flower-visiting honey bees in those fields. Honey bees affected yield, but the effect depended on cultivar type (p = 0.04). Post-hoc analysis revealed that open-pollinated cultivars, but not hybrid cultivars, had 11% higher yields in fields with added honey bees than those grown in the control fields (p = 0.07). To our knowledge, this is the first whole-field study in replicated landscapes to assess the benefit of insect pollination in oilseed rape. Our results demonstrate that honey bees have the potential to increase oilseed rape yields, thereby emphasizing the importance of pollinator management for optimal cultivation of oilseed rape.

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References

  • Abrol DP (2007) Honeybees and rapeseed: a pollinator-plant interaction. In: Gupta SK, Kader JC (eds) Advances in botanical research. Academic Press, London, pp 337–367. doi:10.1016/S0065-2296(07)45012-1

    Google Scholar 

  • Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:1–4. doi:10.1016/j.cub.2009.03.071

    Article  Google Scholar 

  • Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, Cane J, Allen Cox P, Dalton V, Feinsinger P, Ingram M, Inouye D, Jones E, Kennedy K, Kevan P, Koopowitz H, Medellin R, Medellin-Morales S, Nabhan GP, Pavlik B, Tepedino V, Torchio P, 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:10.1111/j.1523-1739.1998.97154.x

    Article  Google Scholar 

  • Aras P, De Oliveira D, Savoie L (1996) Effect of a honey bee (Hymenoptera: Apidae) gradient on the pollination and yield of lowbush blueberry. J Econ Entomol 89:1080–1083

    Article  Google Scholar 

  • Bartomeus I, Potts SG, Steffan-Dewenter I, Vaissière BE, Woyciechowski M, Krewenka KM, Tscheulin T, Roberts SPM, Szentgyörgyi H, Westphal C, Bommarco R (2014) Contribution of insect pollinators to crop yield and quality varies with agricultural intensification. PeerJ 2:e328. doi:10.7717/peerj.328

    Article  PubMed  PubMed Central  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0-6. Available at: http://CRAN.R-project.org/package=lme4

  • Becker HC, Damgaard C, Karlsson B (1992) Environmental variation for outcrossing rate in rapeseed (Brassica napus). Theor Appl Genet 84:303–306. doi:10.1007/bf00229487

    CAS  PubMed  Google Scholar 

  • Becker HC, Löptien H, Röbbelen G (1999) Breeding: an overview. In: Gomez-Campo C (ed) Biology of Brassica coenospecies. Elsevier, Amsterdam

    Google Scholar 

  • Bell SA, Cresswell JE (1998) The phenology of gender in homogamous flowers: temporal change in the residual sex function of flowers of oil-seed rape (Brassica napus). Funct Ecol 12:298–306. doi:10.1046/j.1365-2435.1998.00190.x

    Article  Google Scholar 

  • Bolker MB, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2011) GLMMs in action: gene-by-environment interaction in total fruit production of wild populations of Arabidopsis thaliana. Revised version 1. New York. Available at: http://glmm.wdfiles.com/local–files/examples/Banta_2011_part1.pdf

  • Bos MM, Veddeler D, Bogdanski AK, Klein A-M, Tscharntke T, Steffan-Dewenter I, Tylianakis JM (2007) Caveats to quantifying ecosystem services: fruit abortion blurs benefits from crop pollination. Ecol Appl 17:1841–1849. doi:10.1890/06-1763.1

    Article  PubMed  Google Scholar 

  • Breeze TD, Vaissière BE, Bommarco R, Petanidou T, Seraphides N, Kozák L, Scheper J, Biesmeijer JC, Kleijn D, Gyldenkærne S, Moretti M, Holzschuh A, Steffan-Dewenter I, Stout JC, Pärtel M, Zobel M, Potts SG (2014) Agricultural policies exacerbate honeybee pollination service supply-demand mismatches across Europe. PLoS One 9:e82996. doi:10.1371/journal.pone.0082996

    Article  PubMed  PubMed Central  Google Scholar 

  • Cresswell JE, Osborne JL, Bell SA (2002) A model of pollinator-mediated gene flow between plant populations with numerical solutions for bumblebees pollinating oilseed rape. Oikos 98:375–384. doi:10.1034/j.1600-0706.2002.980302.x

    Article  Google Scholar 

  • Cunningham SA, Le Feuvre D (2013) Significant yield benefits from honeybee pollination of faba bean (Vicia faba) assessed at field scale. Field Crop Res 149:269–275. doi:10.1016/j.fcr.2013.05.019

    Article  Google Scholar 

  • Diepenbrock W (2000) Yield analysis of winter oilseed rape (Brassica napus L.): a review. Field Crop Res 67:35–49. doi:10.1016/s0378-4290(00)00082-4

    Article  Google Scholar 

  • Dupont YL, Damgaard C, Simonsen V (2011) Quantitative historical change in bumblebee (Bombus spp.) assemblages of red clover fields. PLoS One 6:e25172. doi:10.1371/journal.pone.0025172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durán XA, Ulloa RB, Carrillo JA, Contreras JL, Bastidas MT (2010) Evaluation of yield component traits of honeybee pollinated (Apis mellifera L.) rapeseed canola (Brassica napus L.). Chil J Agric Res 70:309–314

    Google Scholar 

  • FAO (2014) FAOSTATS: Food and Agricultural Organization of the United Nations 2013 Statistical division. Available at: http://faostat.fao.org/ default.aspx. Accessed 26 June 2014

  • Fox J (2003) Effect displays in R for generalised linear models. J Stat Softw 8:1–27

    Article  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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 S, Ricketts TH, Szentgyörgyi H, Viana BF, Westphal C, Winfree R, Klein A-M (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

    Article  PubMed  Google Scholar 

  • Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein A-M (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611. doi:10.1126/science.1230200

    Article  CAS  PubMed  Google Scholar 

  • Gelman A, Su YS (2013) arm: data analysis using regression and multilevel/hierarchical models. R package version 1.6-10. Available at: http://CRAN.R-project.org/package=arm

  • Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. doi:10.1126/science.1255957

    Google Scholar 

  • Grosse F, Leon J, Diepenbrock W (1992) Yield formation and yield structure of winter oilseed rape (Brassica-napus L.). 1. Genotypic variability. J Agron Crop Sci 169:70–93

    Article  Google Scholar 

  • 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 

  • Hoyle M, Cresswell JE (2007) The effect of wind direction on cross-pollination in wind-pollinated GM crops. Ecol Appl 17:1234–1243. doi:10.1890/06-0569

    Article  PubMed  Google Scholar 

  • Hoyle M, Hayter K, Cresswell JE (2007) Effect of pollinator abundance on self-fertilization and gene flow: application to GM canola. Ecol Appl 17:2123–2135. doi:10.1890/06-1972.1

    Article  PubMed  Google Scholar 

  • Hudewenz A, Pufal G, Bögeholz A-L, Klein A-M (2013) Cross-pollination benefits differ among oilseed rape varieties. J Agric Sci 152:770–778. doi:10.1017/S0021859613000440

    Article  Google Scholar 

  • 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 24:547–555. doi:10.1007/s10980-009-9331-2

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kamler F, Jas S (2003) Influence of pollination by honey bee on seed yield on selected cultivars of winter rape. J Apic Sci 47:119–125

    Google Scholar 

  • Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colarado, Colarado

    Google Scholar 

  • Klein A-M, Vaissière 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 Biol Sci 274:303–313. doi:10.1098/rspb.2006.3721

    Article  Google Scholar 

  • Koltowski Z (2005) The effect of pollinating insects on the yield of winter rapeseed (Brassica napus L. var. napus f. biennis) cultivars. J Apic Sci 49:29–41

    Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2013) lmerTest: Tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R package version 2.0-6. Available at: http://CRAN.R-project.org/package=lmerTest

  • Lankinen Å, Larsson MC (2007) Conflicting selection pressures on reproductive functions and speciation in plants. Evol Ecol 23:147–157. doi:10.1007/s10682-007-9227-z

    Article  Google Scholar 

  • Lenth RV (2013) lsmeans: Least-squares means. R package version 1.10-2. Available at: http://CRAN.R-project.org/package=lsmeans

  • Marini L, Tamburini G, Petrucco-Toffolo E, Lindström SAM, Zanetti F, Mosca G, Bommarco R (2015) Crop management modifies the benefits of insect pollination in oilseed rape. Agric Ecosyst Environ 207:61–66. doi:10.1016/j.agee.2015.03.027

    Article  Google Scholar 

  • Mayer C, Adler L, Armbruster WS, Dafni A, Eardley C, Huang S-Q, Kevan PG, Ollerton J, Packer L, Ssymank A, Stout JC, Potts SG (2011) Pollination ecology in the 21st century: key questions for future research. J Pollinat Ecol 3:8–23

    Google Scholar 

  • McGregor DI (1987) Effect on plant density on development and yield of rapeseed and its significance to recovery from hail injury. Can J Plant Sci 67:43–51. doi:10.4141/cjps87-005

    Article  Google Scholar 

  • 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 

  • Olsson G (1960) Self-incompatibility and outcrossing in rape and white mustard. Hereditas 46:241–252. doi:10.1111/j.1601-5223.1960.tb03085.x

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org

  • 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

    Article  PubMed  Google Scholar 

  • Sabbahi R, De Oliveira D, 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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Stanley DA, Gunning D, Stout JC (2013) Pollinators and pollination of oilseed rape crops (Brassica napus L.) in Ireland: ecological and economic incentives for pollinator conservation. J Insect Conserv 17:1181–1189. doi:10.1007/s10841-013-9599-z

    Article  Google Scholar 

  • Steffan-Dewenter I (2003) Seed set of male-sterile and male-fertile oilseed rape (Brassica napus) in relation to pollinator density. Apidologie 34:227–235. doi:10.1051/apido:2003015

    Article  Google Scholar 

  • Tommasini L, Batley J, Arnold GM, Cooke RJ, Donini P, Lee D, Law JR, Lowe C, Moule C, Trick M, Edwards KJ (2003) The development of multiplex simple sequence repeat (SSR) markers to complement distinctness, uniformity and stability testing of rape (Brassica napus L.) varieties. Theor Appl Genet 106:1091–1101. doi:10.1007/s00122-002-1125-8

    CAS  PubMed  Google Scholar 

  • Vaissiere BE, Freitas BM, Gemmill-Herren B (2011) Protocol to detect and assess pollination deficits in crops: a handbook for its use. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Williams IH, Martin AP, White RP (1986) The pollination requirements of oil-seed rape (Brassica napus L.). J Agr Sci 106:27–30

    Article  Google Scholar 

  • Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge

    Google Scholar 

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Acknowledgments

We thank the farmers and beekeepers involved in the study. Martin Stjernman and SAPES are thanked for help with statistics and providing landscape data. The study was funded by grants from the Swedish Farmers’ Foundation for Agricultural Research, the Swedish Board of Agriculture, the Swedish Rural Economy and Agricultural Society in Kristianstad, Lund University, Henning and Elsa Anderssons foundation, the Kristianstad foundation to SL and RB, and by the Swedish research council FORMAS to RB and HGS.

Author contribution statement

SL, MR, HGS and RB designed the experiments. SL and LH performed the experiments. SL and HGS analyzed the data with advice from all other authors. SL wrote the manuscript with contributions from the other authors.

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Authors and Affiliations

  1. Department of Ecology, Swedish University of Agriculture Sciences, 750 07, Uppsala, Sweden

    Sandra A. M. Lindström & Riccardo Bommarco

  2. Swedish Rural Economy and Agricultural Society, 291 09, Kristianstad, Sweden

    Sandra A. M. Lindström

  3. Department of Biology, Lund University, 223 62, Lund, Sweden

    Sandra A. M. Lindström, Maj Rundlöf & Henrik G. Smith

  4. Centre for Environmental and Climate Research, Lund University, 223 62, Lund, Sweden

    Lina Herbertsson & Henrik G. Smith

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  1. Sandra A. M. Lindström
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Correspondence to Sandra A. M. Lindström.

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Communicated by Diethart Matthies.

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Lindström, S.A.M., Herbertsson, L., Rundlöf, M. et al. Large-scale pollination experiment demonstrates the importance of insect pollination in winter oilseed rape. Oecologia 180, 759–769 (2016). https://doi.org/10.1007/s00442-015-3517-x

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