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Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees
Open accessAbstract
Recent concern over global pollinator declines has led to considerable research on the effects of pesticides on bees. Although pesticides are typically not encountered at lethal levels in the field, there is growing evidence indicating that exposure to field-realistic levels can have sublethal effects on bees, affecting their foraging behaviour, homing ability and reproductive success. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants, but until now research on pesticide effects has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence to our knowledge that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Bumblebee colonies exposed to a neonicotinoid pesticide provided lower visitation rates to apple trees and collected pollen less often. Most importantly, these pesticide-exposed colonies produced apples containing fewer seeds, demonstrating a reduced delivery of pollination services. Our results also indicate that reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour, but most likely due to effects at the colony level. These findings show that pesticide exposure can impair the ability of bees to provide pollination services, with important implications for both the sustained delivery of stable crop yields and the functioning of natural ecosystems.
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Cites
Modern Applied Statistics with S
Venables, W. N., & Ripley, B. D. (2002) · Statistics and Computing · doi:10.1007/978-0-387-21706-2 · Cited by 24,305
Simultaneous Inference in General Parametric Models
Hothorn, T., Bretz, F., & Westfall, P. (2008) · Biometrical Journal · doi:10.1002/bimj.200810425 · Cited by 13,847
Importance of pollinators in changing landscapes for world crops
Klein, A.-M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2006.3721 · Cited by 7,176
Bee declines driven by combined stress from parasites, pesticides, and lack of flowers
Goulson, D., Nicholls, E., Botías, C., & Rotheray, E. L. (2015) · Science · doi:10.1126/science.1255957 · Cited by 4,033
How many flowering plants are pollinated by animals?
Ollerton, J., Winfree, R., & Tarrant, S. (2011) · Oikos · doi:10.1111/j.1600-0706.2010.18644.x · Cited by 3,874
REVIEW: An overview of the environmental risks posed by neonicotinoid insecticides
Goulson, D. (2013) · Journal of Applied Ecology · doi:10.1111/1365-2664.12111 · Cited by 1,828
A Common Pesticide Decreases Foraging Success and Survival in Honey Bees
Henry, M., Béguin, M., Requier, F., Rollin, O., Odoux, J.-F., Aupinel, P., Aptel, J., Tchamitchian, S., & Decourtye, A. (2012) · Science · doi:10.1126/science.1215039 · Cited by 1,474
Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth and Queen Production
Whitehorn, P. R., O’Connor, S., Wackers, F. L., & Goulson, D. (2012) · Science · doi:10.1126/science.1215025 · Cited by 1,290
Seed coating with a neonicotinoid insecticide negatively affects wild bees
Rundlöf, M., Andersson, G. K. S., Bommarco, R., Fries, I., Hederström, V., Herbertsson, L., Jonsson, O., Klatt, B. K., Pedersen, T. R., Yourstone, J., et al. (2015) · Nature · doi:10.1038/nature14420 · Cited by 1,087
Bateman’s principle and plant reproduction: The role of pollen limitation in fruit and seed set
Burd, M. (1994) · The Botanical Review · doi:10.1007/bf02856594 · Cited by 1,001
Combined pesticide exposure severely affects individual- and colony-level traits in bees
Gill, R. J., Ramos-Rodriguez, O., & Raine, N. E. (2012) · Nature · doi:10.1038/nature11585 · Cited by 998
Self-citationDelivery of crop pollination services is an insufficient argument for wild pollinator conservation
Kleijn, D., Winfree, R., Bartomeus, I., Carvalheiro, L. G., Henry, M., Isaacs, R., Klein, A.-M., Kremen, C., M'Gonigle, L. K., Rader, R., et al. (2015) · Nature Communications · doi:10.1038/ncomms8414 · Cited by 982
Self-citationMultiple Routes of Pesticide Exposure for Honey Bees Living Near Agricultural Fields
Krupke, C. H., Hunt, G. J., Eitzer, B. D., Andino, G., & Given, K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029268 · Cited by 871
Neonicotinoid Residues in Wildflowers, a Potential Route of Chronic Exposure for Bees
Botías, C., David, A., Horwood, J., Abdul-Sada, A., Nicholls, E., Hill, E., & Goulson, D. (2015) · Environmental Science & Technology · doi:10.1021/acs.est.5b03459 · Cited by 457
Spatial and Temporal Trends of Global Pollination Benefit
Lautenbach, S., Seppelt, R., Liebscher, J., & Dormann, C. F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035954 · Cited by 445
Godfray, H. C. J., Blacquière, T., Field, L. M., Hails, R. S., Petrokofsky, G., Potts, S. G., Raine, N. E., Vanbergen, A. J., & McLean, A. R. (2014) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2014.0558 · Cited by 429
Self-citationContribution of Pollinator-Mediated Crops to Nutrients in the Human Food Supply
Eilers, E. J., Kremen, C., Smith Greenleaf, S., Garber, A. K., & Klein, A.-M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021363 · Cited by 422
A meta-analysis comparing the sensitivity of bees to pesticides
Arena, M., & Sgolastra, F. (2014) · Ecotoxicology · doi:10.1007/s10646-014-1190-1 · Cited by 418
Avoiding a bad apple: Insect pollination enhances fruit quality and economic value
Garratt, M. P. D., Breeze, T. D., Jenner, N., Polce, C., Biesmeijer, J. C., & Potts, S. G. (2014) · Agriculture, Ecosystems & Environment · doi:10.1016/j.agee.2013.10.032 · Cited by 348
Self-citationNeonicotinoids Interfere with Specific Components of Navigation in Honeybees
Fischer, J., Müller, T., Spatz, A.-K., Greggers, U., Grünewald, B., & Menzel, R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091364 · Cited by 338
Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure
Gill, R. J., & Raine, N. E. (2014) · Functional Ecology · doi:10.1111/1365-2435.12292 · Cited by 306
Self-citationField realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency
Feltham, H., Park, K., & Goulson, D. (2014) · Ecotoxicology · doi:10.1007/s10646-014-1189-7 · Cited by 285
Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees
Palmer, M. J., Moffat, C., Saranzewa, N., Harvey, J., Wright, G. A., & Connolly, C. N. (2013) · Nature Communications · doi:10.1038/ncomms2648 · Cited by 279
Brittain, C., & Potts, S. G. (2011) · Basic and Applied Ecology · doi:10.1016/j.baae.2010.12.004 · Cited by 263
Self-citationDively, G. P., & Kamel, A. (2012) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf205393x · Cited by 242
Pilling, E., Campbell, P., Coulson, M., Ruddle, N., & Tornier, I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077193 · Cited by 205
Biddinger, D. J., Robertson, J. L., Mullin, C., Frazier, J., Ashcraft, S. A., Rajotte, E. G., Joshi, N. K., & Vaughn, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072587 · Cited by 170
Stewart, S. D., Lorenz, G. M., Catchot, A. L., Gore, J., Cook, D., Skinner, J., Mueller, T. C., Johnson, D. R., Zawislak, J., & Barber, J. (2014) · Environmental Science & Technology · doi:10.1021/es501657w · Cited by 169
Pollination deficits in UK apple orchards
Garratt, M. P. D., Truslove, L., Coston, D. J., Evans, R., Moss, E. D., Dodson, C.-A., Jenner, N., Biesmeijer, J. C., & Potts, S. G. (2013) · Journal of Pollination Ecology · doi:10.26786/1920-7603(2014)8 · Cited by 105
Self-citationSheffield, C. S. (2014) · Journal of Pollination Ecology · doi:10.26786/1920-7603(2014)11 · Cited by 63
Volz, R. K., Tustin, D. S., & Ferguson, I. B. (1996) · Scientia Horticulturae · doi:10.1016/s0304-4238(96)00934-x · Cited by 50
Fine-scale flower-visiting behavior revealed by using a high-speed camera
Sakamoto, R. L., Morinaga, S., Itô, M., et al. (2012) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-011-1314-z · Cited by 16
Cited by
Safeguarding pollinators and their values to human well-being
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., et al. (2016) · Nature · doi:10.1038/nature20588 · Cited by 2,138
Self-citationTrends in Global Agricultural Land Use: Implications for Environmental Health and Food Security
Ramankutty, N., Mehrabi, Z., Waha, K., Jarvis, L., Kremen, C., Herrero, M., & Rieseberg, L. H. (2018) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042817-040256 · Cited by 954
The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013
Wood, T. J., & Goulson, D. (2017) · Environmental Science and Pollution Research · doi:10.1007/s11356-017-9240-x · Cited by 623
Pesticides have negative effects on non-target organisms
Wan, N.-F., Fu, L., Dainese, M., Kiær, L. P., Hu, Y.-Q., Xin, F., Goulson, D., Woodcock, B. A., Vanbergen, A. J., Spurgeon, D. J., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-56732-x · Cited by 432
Global Trends in Bumble Bee Health
Cameron, S. A., & Sadd, B. M. (2020) · Annual Review of Entomology · doi:10.1146/annurev-ento-011118-111847 · Cited by 367
Metadata
- Authors
- Stanley, D. A., Garratt, M. P. D., Wickens, J. B., Wickens, V. J., Potts, S. G., & Raine, N. E.
- Venue
- Nature
- Published
- 2015-11-18
- Volume
- 528
- Issue
- 7583
- Pages
- 548-550
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2176676002
- Cited by
- 369
- References
- 32
- FWCI
- 25.73
- Type
- journal article
- Language
- en
- Open access
- green
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