Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees

Nature

Volumn 528, Issue 7583, 2015, Pages 548-550

  Stanley, Dara A ^a   Garratt, Michael P D ^b   Wickens, Jennifer B ^b   Wickens, Victoria J ^b   Potts, Simon G ^b   Raine, Nigel E ^a,c  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

^c UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

IMIDACLOPRID; NEUROTRANSMITTER RECEPTOR; THIAMETHOXAM; INSECTICIDE;

BEE; CROP YIELD; ECOSYSTEM FUNCTION; FORAGING BEHAVIOR; FRUIT; HOMING BEHAVIOR; NEONICOTINOID PESTICIDE; POLLEN; POLLINATION; POLLINATOR; REPRODUCTIVE SUCCESS;

ANGIOSPERM; ANIMAL BEHAVIOR; APPLE; ARTICLE; BUMBLEBEE; ENVIRONMENTAL EXPOSURE; FLOWER; FORAGING; HARVEST; NONHUMAN; POLLEN; POLLINATION; PRIORITY JOURNAL; ANIMAL; BEE; CROP; DRUG EFFECTS; FRUIT; GROUP PROCESS; MALUS; PHYSIOLOGY; PLANT SEED;

APOIDEA; MAGNOLIOPHYTA; MALUS X DOMESTICA;

ANIMALS; BEES; BEHAVIOR, ANIMAL; CROPS, AGRICULTURAL; FRUIT; GROUP PROCESSES; INSECTICIDES; MALUS; POLLEN; POLLINATION; SEEDS;

EID: 84951320604     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16167     Document Type: Article

References (42)

1. Gill, R. J., Ramos-Rodriguez, O. & Raine, N. E. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105-108 (2012).
2. Whitehorn, P. R., O'Connor, S., Wäckers, F. L. & Goulson, D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351-352 (2012).
3. Godfray, H. C. J. et al. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. R. Soc. Lond. B 281, 20140558 (2014).
4. Arena, M. & Sgolastra, F. A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23, 324-334 (2014).
5. Rundlöf, M. et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521, 77-80 (2015).
6. Feltham, H., Park, K. & Goulson, D. Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23, 317-323 (2014).
7. Gill, R. J. & Raine, N. E. Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Funct. Ecol. 28, 1459-1471 (2014).
8. Henry, M. et al. A common pesticide decreases foraging success and survival in honey bees. Science 336, 348-350 (2012).
9. Fischer, J. et al. Neonicotinoids interfere with specific components of navigation in honeybees. PLoS One 9, e91364 (2014).
10. Klein, A. M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. Lond. B 274, 303-313 (2007).
11. Ollerton, J., Winfree, R. & Tarrant, S. How many flowering plants are pollinated by animals? Oikos 120, 321-326 (2011).
12. Kleijn, D. et al. Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat. Commun. 6, 7414 (2015).
13. Eilers, E. J., Kremen, C., Greenleaf, S. S., Garber, A. K. & Klein, A. M. Contribution of pollinator-mediated crops to nutrients in the human food supply. PLoS One 6, e21363 (2011).
14. Lautenbach, S., Seppelt, R., Liebscher, J. & Dormann, C. F. Spatial and temporal trends of global pollination benefit. PLoS One 7, e35954 (2012).
15. Goulson, D. An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 50, 977-987 (2013).
16. Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).
17. Brittain, C. & Potts, S. G. The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic Appl. Ecol. 12, 321-331 (2011).
18. Sheffield, C. S. Pollination, seed set and fruit quality in apple: studies with Osmia lignaria (Hymenoptera: Megachilidae) in the Annapolis Valley, Nova Scotia, Canada. J. Pollinat. Ecol. 12, 120-128 (2014).
19. Garratt, M. P. D. et al. Pollination deficits in UK apple orchards. J. Pollinat. Ecol. 12, 9-14 (2014).
20. Palmer, M. J. et al. Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nat. Commun. 4, 1634 (2013).
21. Déglise, P., Grünewald, B. & Gauthier, M. The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells. Neurosci. Lett. 321, 13-16 (2002).
22. Cutler, G. C. & Rix, R. R. Can poisons stimulate bees? Appreciating the potential of hormesis in bee-pesticide research. Pest Manag. Sci. 71, 1368-1370 (2015).
23. Sakamoto, R. L., Morinaga, S.-I., Ito, M. & Kawakubo, N. Fine-scale flower-visiting behavior revealed by using a high-speed camera. Behav. Ecol. Sociobiol. 66, 669-674 (2012).
24. Castro, S., Loureiro, J., Ferrero, V., Silveira, P. & Navarro, L. So many visitors and so few pollinators: variation in insect frequency and effectiveness governs the reproductive success of an endemic milkwort. Plant Ecol. 214, 1233-1245 (2013).
25. Buccheri, M. & Di Vaio, C. Relationship among seed number, quality, and calcium content in apple fruits. J. Plant Nutr. 27, 1735-1746 (2004).
26. Garratt, M. P. D. et al. Avoiding a bad apple: Insect pollination enhances fruit quality and economic value. Agric. Ecosyst. Environ. 184, 34-40 (2014).
27. Volz, R. K., Tustin, D. S. & Ferguson, I. B. Pollination effects on fruit mineral composition, seeds and cropping characteristics of 'Braeburn' apple trees. Sci. Hortic. (Amsterdam) 66, 169-180 (1996).
28. Biddinger, D. J. et al. Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS One 8, e72587 (2013).
29. Decourtye, A., Henry, M. & Desneux, N. Environment: overhaul pesticide testing on bees. Nature 497, 188 (2013).
30. Burd, M. Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot. Rev. 60, 83-139 (1994).
31. Thompson, H. et al. Effects of neonicotinoid seed treatments on bumble bee colonies under field conditions. (Food and Environment Research Agency (FERA), 2013).
32. Pilling, E., Campbell, P., Coulson, M., Ruddle, N. & Tornier, I. A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam. PLoS One 8, e77193 (2013).
33. Castle, S. J., Byrne, F. J., Bi, J. L. & Toscano, N. C. Spatial and temporal distribution of imidacloprid and thiamethoxam in citrus and impact on Homalodisca coagulata populations. Pest Manag. Sci. 61, 75-84 (2005).
34. Dively, G. P. & Kamel, A. Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. J. Agric. Food Chem. 60, 4449-4456 (2012).
35. Botías, C. et al. Neonicotinoid residues in wildflowers, a potential route of chronic exposure for bees. Environ. Sci. Technol. 9, 12731-12740 (2015).
36. Krupke, C. H., Hunt, G. J., Eitzer, B. D., Andino, G. & Given, K. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One 7, e29268 (2012).
37. Stewart, S. D. et al. Potential exposure of pollinators to neonicotinoid insecticides from the use of insecticide seed treatments in the mid-southern United States. Environ. Sci. Technol. 48, 9762-9769 (2014).
38. R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org (2011).
39. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Development Core Team. Package "nlme": Linear and nonlinear mixed effects models. R package version 3.1-104 (2012).
40. Bates, D., Maechler, M., Bolker, B. & Walker, S. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7 http://CRAN.R-project.org/package= lme4 (2014).
41. Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S. 4th edn (Springer, 2002).
42. Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom. J. 50, 346-363 (2008).