Abstract
This is the first report showing that using honeybee (Apis mellifera) and wild pollinators complementary pollination can enhance soybean productivity (Glycine max). Current industrial production of soybean involves autopollination and high loads of pesticides. Therefore, growers have neglected possible biotic pollination despite suggestions that soybean benefit from insect pollinators. Reports advocating possible biotic pollination are based on experiments where bees are caged with flowering plants and the absence of pesticides, thus not in field conditions. Therefore, here we compared in field conditions soybean yield produced (1) independently of biotic pollinators, (2) with wild pollinators and (3) with honeybee colonies. Results showed an increase of +6.34 % of soybean yield in areas where wild pollinators had free access to flowers. The introduction of honeybee colonies further raised the yield of +18.09 %. Our findings therefore show that, though soybean is autogamous, allowing pollination by wild pollinators leads to higher yields. Moreover, adding honeybee mitigates pollination deficits and improves yield compared to current practices.
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References
Barret SCH, Harder LD, Cole WW (1994) Effects of flower number and position on self-fertilization in experimental populations of Eichhornia paniculata (Pontederiacea). Funct Ecol 8:526–535
Carlson JB, Lersten NR (1987) Reproductive morphology. In: Wilcox JR (ed) Soybeans: improvement, production and uses, agronomy monograph, 16. ASA, Madison, pp 95–134
Chacoff NP, Morales CL, Garibaldi LA, Ashworth L, Aizen MA (2010) Pollinator dependence of Argentinean agriculture: current status and temporal analysis. Americas J Plant Sci Biotech 3:106–116
Chiari WC, Toledo VDAAD, Ruvolo-Takasusuki MCC, Oliveira AJBD, Sakaguti ES, Attencia VM, Costa FM, Mitsiu MH (2005) Pollination of soybean (Glycine max (L.) Merril by honeybees (Apis mellifera L.). Braz Arch Biol Technol 48:31–36
Cruz DO, Freitas BM, Silva LA, Silva EMS, Bomfim IGA (2005) Pollination efficiency of the stingless bee Melipona subnitida on greenhouse sweet pepper. Pesqui Agropec Bras 40:1197–1201
Delaplane KS, Mayer DF (2000) Crop pollination by bees. CABI Publishing, New York
DNOCS (2011) Perímetro irrigado Jaguaribe-Apodi 2011. Departamento Nacional de Obras Contra as Secas. http://www.dnocs.gov.br/~dnocs/doc/canais/perimetros_irrigados/ce/ Jaguaribe_apodi.html>. Accessed June 20 2011
Embrapa (2005) BRS Carnaúba, nova cultivar de soja para a região Norte e Nordeste do Brasil. Comunicado Técnico 180. Embrapa-Meio Norte, Teresina
Erickson EH, Berger GA, Shannon JG, Robin JM (1978) Honey bee pollination increases soybean yields in the Mississippi delta region of Arkansas and Missouri. Econ Entomol 71:601–603
FAO (2012) FAOSTAT: production, crops, soybean, 2010 data. http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567 #ancor. Accessed Oct 04 2012
Fargione J, Hill J, Tilman D, Polasky S, Hawthorne P (2008) Land clearing and the biofuel carbon debt. Science 319:1235–1238
Fehr WR (1980) Soybean. In: Fehr WR, Hadley H (eds) Hybridization of crop plants. Am Soc Agron, Madison, pp 589–599
Free JB (1993) Insect pollination of crops, 2nd edn. University Press, Cardiff
Freitas BM, Imperatriz-Fonseca VL, Medina LM, Kleinert AMP, Galetto L, Nates-Parra G, Quezada-Euán JJG (2009) Diversity, threats and conservation of native bees in the Neotropics. Apidologie 40:332–346
Gallai N, Salles JM, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of the world agriculture confronted with pollination decline. Ecol Econ 68:810–821
Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham AS, 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 K, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TA, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein AM (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611. doi:10.1126/science.1230200
Klein AM, Steffan-Dewenter I, Tscharntke T (2003) Bee pollination and fruit set of Coffea Arabica and C. canephora (Rubiaceae). Am J Bot 90:153–157
Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunnigham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313
Lautenbach S, Seppelt R, Liebscher J, Dormann CF (2012) Spatial and temporal trends of global pollination benefit. PLoS ONE 7:e35954
Masuda T, Goldsmith PD (2009) World soybean production: area harvested, yield, and long-term projections. Int Food Agribus Manag Rev 12:143–162
McGregor SE (1976) Insect pollination of cultivated crop plants. USDA, Tucson
Milfont MO (2012) Uso da abelha melífera (Apis mellifera L.) na polinização e aumento de produtividade de grãos em variedade de soja (Glycine max (L.) Merril.) adaptada às condições climáticas do nordeste brasileiro. Thesis, Universidade Federal do Ceará
Monsanto (2011) Maximizing soybean yield potential. Agronomic spotlight. Monsanto technology development. http://www.renkseed.com/Portals/0/Agronomic%20Spotlight%20-%20Maximizing%20Soybean%20Yield%20Potential.pdf. Accessed Oct 04 2012
Rizzardo RAG, Milfont MO, Silva EMS, Freitas BM (2012) Apis mellifera pollination improves agronomic productivity of anemophilous castor bean (Ricinus communis). An Acad Bras Cienc 84:605–608
Robacker DC, Flottum PK, Sammataro D, Erickson EH (1983) Effects of climatic and edaphic factors on soybean flowers and on the subsequent attractiveness of the plants to honey bees. Field Crop Res 6:267–278
Rust RW, Macon CE, Erickson EH (1980) Wild bees on soybeans, Glycine max. Environ Entomol 9:230–232
USSEC (2008) How the global oilseed and grain trade works. USSEC, Saint Louis
Vaissière BE, Freitas BM, Gemmill-Herren B (2011) Protocol to detect and assess pollination deficits in crops: a handbook for its use. FAO, Rome
Yoshimura Y (2011) Wind tunnel and field assessment of pollen dispersal in soybean [Glycine max (L.) Merr.]. J Plant Res 124:109–114
Yoshimura Y, Matsuo K, Yasuda K (2006) Gene flow from GM glyphosate-tolerant to conventional soybeans under field conditions in Japan. Environ Biosafety Res 5:169–173
Acknowledgments
Authors thank Faedo Sementes for permission to carry out this study in its soybean plantations, Altamira Apícola for lending the honeybee colonies, David R. Rocha for processing the figures of this article and the National Council for Scientific and Technological Development—CNPq, Brasília-Brazil for the D.Sc. scholarship to M.O. Milfont and the research fellowship to B.M. Freitas (proc. # #305062/2007-7).
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de O. Milfont, M., Rocha, E.E.M., Lima, A.O.N. et al. Higher soybean production using honeybee and wild pollinators, a sustainable alternative to pesticides and autopollination. Environ Chem Lett 11, 335–341 (2013). https://doi.org/10.1007/s10311-013-0412-8
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DOI: https://doi.org/10.1007/s10311-013-0412-8