Influence of Wild Bee Diversity on Canola Crop Yields

Rosana Halinski, Charles Fernando dos Santos, Tatiana Guterres Kaehler, Betina Blochtein


The foraging range of bees determines the spatial scale over which each species can provide pollination services. In agricultural ecosystems, productivity is related not only to the taxonomic diversity of bees per se, but also to the location of their nesting sites, which reflects on their flying range. Within this context, the present study sought to assess how wild bee assemblages affect the yield of Brassica napus at three different distances (25 m, 175 m, 325 m) from forest remnants in Southern Brazil. Bees were sampled by means of pan traps and findings were analyzed using the Shannon diversity index and generalized linear models. We identified 11 species of native bees, both solitary and social, as well as the exotic species Apis mellifera, which was most abundant. Our findings show that canola crop yield were positively influenced by the diversity of bee species. This demonstrates that native bees, not only A. mellifera, can contribute significantly to the productivity of canola crops. In addition, we found that bee body size is significantly associated with flight distance traveled within the canola fields, and demonstrated a relationship with nesting sites. Thus, we hypothesize that canola yields are associated with the presence of wild bee species, both social and solitary, and that maintenance of these pollinators is directly dependent on practices adopted in rural areas, whether within plantation fields per se or in forest remnants used as nesting sites by wild bees.


Brassica napus; pollination; stingless bees; Apis mellifera; agricultural ecosystems

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Abrol, D. P. (2007). Honeybees and rapeseed: a pollinator-plant interaction. Advances in Botanical Research, 45: 337–367. doi: 10.1016/S0065-2296(07)45012-1.

Alvares, C. A., Stape, J. L., Sentelhas, P. C., Gonçalves, J. L. M. & Sparovek, G. (2013). Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22: 711–728. doi: 10.1127/0941-2948/2013/0507.

Araujo, E. D., Costa, M., Chaud-Netto, J. & Fowler, H.G. (2004). Body size and flight distance in stingless bees (Hymenoptera: Meliponini): Inference of flight range and possible ecological implications. Brazilian Journal of Biology, 64: 563-568. doi: 10.1590/S1519-69842004000400003.

Bailey, S., Requier, F., Nusillard, B. & Bouget, C. (2014). Distance from forest edge affects bee pollinators in oilseed rape fields. Ecology and Evolution, 4(4): 370–380. doi: 10.1002/ece3.924.

Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, page in press. doi: 10.18637/jss.v067.i01.

Beekman, M. & Ratnieks, F. L. W. (2000). Long-range foraging by the honey-bee, Apis mellifera L. Functional Ecology, 14: 490-496. doi: 10.1046/j.1365-2435.2000.00443.x.

Becker, H.C., Damgaard, C. & Karlsson, B. (1992) Environmental variation for outcrossing rate in rapeseed (Brassica napus). Theoretical and Applied Genetics, 84: 303-306. doi: 10.1007/BF00229487

Blochtein, B., Nunes-Silva, P., Halinski, R., Lopes, L. A. & Witter, S. (2014). Comparative study of the floral biology and of the response of productivity to insect visitation in two rapeseed cultivars (Brassica napus L.) in Rio Grande do Sul. Brazilian Journal of Biology, 74(4): 784-794. doi: 10.1590/1519-6984.02213.

Bommarco, R., Marini, L. & Vaissière, B. E. (2012). Insect pollination enhances seed yield,quality, and market value in oilseed rape. Oecologia, 169(4): 1025–1032. doi: 10.1007/s00442-012-2271-6.

Bullock, S.H. (1999). Relationships among body size, wing size and mass in bees from a tropical dry forest in Mexico. Journal of the Kansas Entomological Society, 72: 426–439.

Chao, A., Gotelli, N. J., Hsieh, T.C., Sander, E.L., Ma, K. H., Colwell, R. K. & Ellison, A. M. (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs, 84, 45–67. doi: 10.1890/13-0133.1.

Cresswell, J. E. & Osborne, J. L. (2004). The effect of patch size and separation on bumblebee foraging in oilseed rape: implications for gene flow. Journal of Applied Ecology, 41: 539–546. doi: 10.1111/j.0021-8901.2004.00912.x.

CONAB - Companhia Nacional de Abastecimento (2016). Available from:

Corbett, S. A., Williams, I. H., Osborne, J. L. (1991). Bees and the pollination of crops and wild flowers in the European Community. Bee World, 72: 47–59.

D'Ávila, M.; Marchini, L.C. (2005). Pollination provided by bees in economically important crops in Brazil. Boletim da Indústria Animal, 62: 79-90.

Dalmazzo, M. & Roig-Alsina, A. (2012). Nest structure and notes on the social behavior of Augochlora amphitrite (Schrottky) (Hymenoptera, Halictidae). Journal of Hymenoptera Research, 26: 17–29. doi: 10.3897/jhr.26.2440.

Durán, X. A., Ulloa, R. B., Carrillo, J. A., Contreras, J. L. & Bastidas, M. T. (2010). Evaluation of yield component traits of honeybee-pollinated (Apis mellifera L.) rapeseed canola (Brassica napus L.). Chilean Journal of Agricultural Research, 70(2): 309–314.

Eickwort, G. C. & Sakagami, S. F. (1979). A classification of nest architecture of bees in the tribe Augochlorini (Hymenoptera: Halictidae; Halictinae), with descriptions of a Brazilian nest of Rhynocorynura inflaticeps. Biotropica, 11(1): 28–38.

FAO – Food and Agriculture Organization of the United Nations (2010). Available from:

Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., et al. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339: 1608–1611. doi: 10.1126/science.1230200.

Giannini, T. C., Garibaldi, L. A., Acosta, A. L., Silva, J. S., Maia, K. P., Saraiva, A. M., Guimarães Jr., P. R. & Kleinert, A. M. P. (2015). Native and non-native supergeneralist bee species have different effects on plant-bee networks. PLoS ONE, 10(9): 1 – 13. doi: 10.1371/journal.pone.0137198.

Greenleaf, S. S., Williams, N.M., Winfree, R. & Kremen, C. (2007). Bee foraging ranges and their relationship to body size. Oecologia, 153: 589-596.

Halinski, R., Dorneles, A.L. & Blochtein, B. (2015). Bee assemblage in habitats associated with Brassica napus L. Revista Brasileira de Entomologia, 59: 222–228. doi: 10.1016/j.rbe.2015.07.001.

Hervé, M. (2015) ‘RVAideMemoire: Diverse basic statistical and graphical functions’. Available at:

Hill, M.O. (1973) Diversity and evenness: A unifying notation and its consequences. Ecology, 54, 427–432.

Holzschuh, A., Dainese, M., González-Varo, J. P., Mudri-Stojnic, S., Riedinger, V., Rundlöf, M., Scheper, J., Wickens, J. B., Wickens, V. J., Bommarco, R., Kleijn, D. Potts, S. G., Roberts, S. P. M., Smith, H. G., Vilà, M., Vujic, A. & Steffan-Dewenter, I. (2016). Mass-flowering crops dilute pollinator abundance in agricultural landscapes across Europe. Ecology Letters, 19: 1228–1236. doi: 10.1111/ele.12657.

Hsieh, T.C., Ma, K.H. & Chao, A. (2016) iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.12 URL:

Jauker, F., Bondarenko, B., Becker, H.C. & Steffan-Dewenter, I. (2012). Pollination effi ciency of wild bees and hoverfl ies provided to oilseed rape. Agricultural and Forest Entomology, 14: 81-87. doi: 10.1111/j.1461-9563.2011.00541.x.

Klein, A. M., Vaissière, B. E., Cane, J. H., Steffan- Dewenter, I., Cunningham, S. A., Kremen C. & Tscharntke T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society of London B, 274: 303–313. doi: 10.1098/rspb.2006.3721.

Koh, I., Lonsdorf, E.V., Williams, N.M., Brittain, C., Isaacs, R., Gibbs, J. & Ricketts, T.H. (2016) Modeling the status, trends and impacts of wild bee abundance in the United States. Proceedings of the National Academy of Sciences, 113: 140–145. doi: 10.1073/pnas.1517685113.

Kremen, C. (2005). Managing ecosystem services: what do we need to know about their ecology? Ecology Letters, 8: 468–479. Doi: 10.1111/j.1461-0248.2005.00751.x.

Kremen, C., Colwell, R. K., Erwin, T. L., Murphy, D. D., Noss, R. F. & Sanjayan, M. A. (1993). Terrestrial arthropod assemblages: their use in conservation planning. Conservation Biology, 7: 796–808.

Lefcheck, J. S. (2015). PiecewiseSEM: Piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods in Ecology and Evolution, 7: 573-579.

Marjanović-Jeromela, A., Marinkovic, R., Mijic, A., Zdunic, Z., Ivanovska, S., Jankulovska, M. (2008). Correlation and path analysis of quantitative traits in winter rapeseed (Brassica napus L.). Agriculturae Conspectus Scientificus, 73: 13–18.

Morandin, L. A., Winston, M. L., Abbott, V. A. & Franklin, M. T. (2007). Can pastureland increase wild bee abundance in agriculturally intense areas? Basic and Applied Ecology 8: 117-124. doi: 10.1016/j.baae.2006.06.003.

Nieh, J. C., Barreto, L. S., Contrera, F. A. L. & Imperatriz-Fonseca, V. L. (2004). Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes. Proceedings of the Royal Society of London B, 271: 1633–1640. doi: 10.1098/rspb.2004.2717.

Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Henry, M., Stevens, H., Szoecs, E. & Wagner, H. (2016). Community Ecology Package. Package ‘vegan’.

Ollerton, J. & Watts S. (2012). Pollination ecology of the invasive tree tobacco Nicotiana glauca: comparisons across native and non-native ranges. Journal of Pollination Ecology, 9: 85–95.

Peet, R. K. (1974). The measurements of species diversity. Annual Review of Ecology and Systematics, 5: 285-307.

Potts, S. G., Imperatriz-Fonseca, V., Ngo, H. T., Aizen, M. A., Biesmeijer, J. C., Breeze, T. D., Dicks, L. V., Garibaldi, L. A., Hill, R., Settele, J. & Vanbergen, A. J. (2016). Safeguarding pollinators and their values to human well-being. Nature, 540: 220-229. doi: 10.1038/nature20588.

Ricketts, T. H., Regetz, J., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., Bogdanski, A., Gemmill-Herren, B., Greenleaf, S. S., Klein, A. M., Mayfield, M. M., Morandin, L. A., Ochieng, A. & Viana, B. F. (2008). Landscape effects on crop pollination services: are there general patterns? Conservation Biology, 22: 799–801. doi: 10.1111/j.1461-0248.2008.01157.x.

Rosa, A. S., Blochtein, B., Ferreira, N. R., & Witter, S. (2010). Apis mellifera (Hymenoptera: Apidae) as a potencial Brassica napus pollinator (cv. Hyola 432) (Brassicaceae), in Southern Brazil. Brazilian Journal of Biology, 70(4): 1075–1081.

Sabbahi, R., Oliveira, D. de, & Marceau, J. (2005). Influence of honey bee (Hymenoptera: Apidae) density on the production of canola (Crucifera: Brassicacae). Journal of Economic Entomology, 98(2): 367–372.

Samways, M.J. (1995). Insect conservation biology. Chapman & Hall, London.

Veloso, H. P., Oliveira-Filho, L. D., Vaz, A. M. S. F., Lima, M. P. M., Marquete, R. & Brazao, J. E. M. (1992). Manual técnico da vegetacão brasileira. IBGE, Rio de Janeiro.

Vicens, N. & Bosch, J. (2000). Pollinating efficacy of Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae, Apidae) on Red Delicious apple. Environmental Entomology, 29: 235–240. doi: 10.1093/ee/29.2.235.

Vrdoljak, S. M. & Samways, M. J. (2012). Optimising coloured pan traps to survey flower visiting insects. Journal of Insect Conservation, 16: 345–354. doi: 10.1007/s10841-011-9420-9.

Westphal, C., Bommarco, R., Carré, G., Lamborn, E., Morison, N., Petanidou, T., Potts, S. G., Roberts, S. P. M., Szentgyôrgyi, H., Tscheulin, T., Vaissière, B. E., Woyciechowski, M., Biesmeijer, J. C., Kunin, W. E., Settele, J. & Stefan-Dewenter, I. (2008). Measuring bee diversity in different European habitats and biogeographical regions. Ecological Monographs, 78(4): 653–671. doi: 10.1890/07-1292.1.

Witter, S., Nunes-Silva, P., Lisboa, B. B., Tirelli, F. P., Sattler, A., Hilgert-Moreira, S. B. & Blochtein, B. (2015). Stingless bees as alternative pollinators of canola. Journal of Economic Entomology, 1–7. doi: 10.1093/jee/tov096.

Wright, I. R., Roberts, S. P. M. & Collins, B. E. (2015). Evidence of forage distance limitations for small bees (Hymenoptera: Apidae). European Journal of Entomology, 112: 303–310. doi: 10.14411/eje.2015.028.



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