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
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
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
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
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
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
Becker HC, Löptien H, Röbbelen G (1999) Breeding: an overview. In: Gomez-Campo C (ed) Biology of Brassica coenospecies. Elsevier, Amsterdam
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
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
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
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
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
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
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
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
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
Free JB (1993) Insect pollination of crops, 2nd edn. Academic Press, London
Fries I, Stark J (1983) Measuring the importance of honeybees in rape seed production. J Apic Res 22:272–276
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
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
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
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
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
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
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
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
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
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
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
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colarado, Colarado
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Williams IH, Martin AP, White RP (1986) The pollination requirements of oil-seed rape (Brassica napus L.). J Agr Sci 106:27–30
Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge
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.
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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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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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DOI: https://doi.org/10.1007/s00442-015-3517-x