An overview of the environmental risks posed by neonicotinoid insecticides

Journal of Applied Ecology

Volumn 50, Issue 4, 2013, Pages 977-987

  Goulson, Dave ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Bee; Clothianidin; Environmental fate; Half life; Imidacloprid; Non target wildlife; Soil water; Systemic insecticide

Indexed keywords

ARTHROPOD; BIOACCUMULATION; COLONY STRUCTURE; CONCENTRATION (COMPOSITION); ECOSYSTEM SERVICE; ENVIRONMENTAL RISK; HORTICULTURE; INSECTICIDE; MORTALITY; PEST CONTROL; PLANT-POLLINATOR INTERACTION; SOIL WATER; SOLUBILIZATION; TAXONOMY; TOXIN;

APOIDEA; ARTHROPODA; AVES; INVERTEBRATA; MAMMALIA; VERTEBRATA;

EID: 84880326483     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/1365-2664.12111     Document Type: Review

References (90)

1. Alexander, A.C., Culp, J.M., Liber, K. & Cessna, A.J. (2007) Effects of insecticide exposure on feeding inhibition in mayflies and oligochaetes. Environmental Toxicology and Chemistry, 26, 1726-1732.
2. Anhalt, J.C., Moorman, T.B. & Koskinen, W.C. (2008) Degradation and sorption of imidacloprid in dissimilar surface and subsurface soils. Journal of Environmental Science and Health B; Pesticides, Food Contaminants and Agricultural Wastes, 43, 207-213.
3. Anon (2001a) Decision No 2455/2001/Ec of the European Parliament and of the Council of 20 November 2001; establishing the list of priority substances in the field of water policy and amending Directive 2000/60/EC. Official Journal of the European Communities, 331, 1-5.
4. Anon (2001b) Evaluation of the New Active Thiacloprid in the New Product Calypso 480 SC Insecticide. National Registration Authority for Agricultural and Veterinary Chemicals, Canberra, Australia.
5. Anon (2001c) Evaluation of the New Active Thiamethoxam in the New Product Cruiser 350 FS Insecticide Seed Treatment. National Registration Authority for Agricultural and Veterinary Chemicals, Canberra, Australia.
6. Anon (2004) Review report for the active substance acetamiprid. European Commission, Health and Consumer Protection Directorate, SANCO/1392/2001 16 June 2004.
7. Anon (2006) Draft assessment Report (DAR) - public version - Initial risk assessment provided by the rapporteur Member State Germany for the existing active substance imidacloprid. Volume 3, Annex B, B.8, February 2006.
8. Anon (2007) Canadian water quality guidelines: imidacloprid. Canadian Council of Ministers of the Environment, ISBN 978-1-896997-71-1.
9. Anon (2009a) Agri-environment schemes in England 2009; a review of results and effectiveness. Natural England, ISBN 978-1-84754-158-1.
10. Anon (2009b) Thiacloprid. Annex VI Dossier. Proposal for harmonized classification and labelling. UK REACH competent authority, Chemicals Regulation Directorate, November 2009.
11. Anon (2012) Addendum 7 of the draft assessment report of 30 December 2005 (relating to volume 1, volume 3 and addendum 6 of 8 February 2008): confirmatory data; imidacloprid. 24 January 2012. Rapporteur Member State, Germany.
12. Bal, R., Naziroglu, M., Turk, G., Okes, Y., Tuncay, K., Etem, E. et al. (2012a) Insecticide imidacloprid induces morphological and DNA damage through oxidative toxicity on the reproductive organs of developing male rats. Cell Biochemistry and Function, 30, 492-499. doi: 10.1002/cbf.2826.
13. Bal, R., Turk, G., Okes, Y., Etem, E., Tuncay, K., Baydas, G. et al. (2012b) Affects of clothianidin exposure on sperm quality, testicular apoptosis and fatty acid deposition in developing male rats. Cell Biology and Toxicology, 28, 187-200. doi 10.1007/s10565-012-9215-0.
14. Baskaran, S., Kookana, R.S. & Naidu, R. (1999) Degradation of bifenthrin, chlorpyrifos and imidacloprid in soil and bedding materials at termiticidal application rates. Pesticide Science, 55, 1222-1228.
15. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemuller, R., Edwards, M., Peeters, T. et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313, 351-354.
16. Biocca, M., Conte, E., Pulcini, P., Marinelli, E. & Pochi, D. (2011) Sowing simulation tests of a pneumatic drill equipped with systems aimed at reducing the emission of abrasion dust from maize dressed seed. Journal of Environmental Science and Health Part B; Pesticides Food Contaminants and Agricultural Wastes, 46, 438-448.
17. Bonmatin, J.M., Moineau, I., Charvet, R., Collin, M.E., Fleche, C. & Bengsch, E.R. (2005). Behavior of imidacloprid in fields. Toxicity for honey bees. Environmental Chemistry: Green Chemistry and Pollutants in Ecosystems (eds E. Lichtfourse, J. Schwarzbauer & D. Robert ). Springer, New York.
18. Brereton, T., Roy, D.B., Middlebrook, I., Botham, M. & Warren, M. (2011) The development of butterfly indicators in the United Kingdom and assessments in 2010. Journal of Insect Conservation, 15, 139-151.
19. Brooks, D.R., Bater, J.E., Clark, S.J., Monteith, D.T., Andrews, C., Corbett, S.J. et al. (2012) Large carabid beetle declines in a United Kingdom monitoring network increases evidence for a widespread loss in insect biodiversity. Journal of Applied Ecology, 49, 1009-1019.
20. Bueno, A.D., Batistela, M.J., Bueno, R.C.O.D., Franca-Neto, J.D., Nishikawa, M.A.N. & Liberio, A. (2011) Effects of integrated pest management, biological control and prophylactic use of insecticides on the management and sustainability of soybeans. Crop Protection, 30, 937-945.
21. Butchart, S.H.M., Walpole, M., Collen, B., van Strien, A., Scharlemann, J.P.W., Almond, R.E.A. et al. (2010) Global biodiversity: indicators of recent declines. Science, 328, 1164-1168.
22. Byrne, F.J. & Toscano, N.C. (2006) Uptake and persistence of imidacloprid in grapevines treated by chemigation. Crop Protection, 25, 831-834.
23. Castle, S.J., Byrne, F.J., Bi, J.L. & Toscano, N.C. (2005) Spatial and temporal distribution of imidacloprid and thiamethoxam in citrus and impact on Homalodisca coagulata (Say) populations. Pesticide Management Science, 61, 75-84.
24. Cox, L., Koskinen, W. & Yen, P. (1998) Influence of soil properties on sorption-desorption of imidacloprid. Journal of Environmental Science and Health, 33, 123-134.
25. Cox, W.J., Shields, E. & Cherney, J.H. (2008) Planting date and seed treatment effects on soybean in the Northeastern United States. Agronomy Journal, 100, 1662-1665.
26. Cresswell, J.E. (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology, 20, 149-157.
27. De Cant, J. & Barrett, M. (2010). Clothianidin registration of prosper T400 seed treatment on mustard seed (oilseed and condiment) and Poncho/Votivo seed treatment on cotton. United States Environmental Protection Agency report, 2 November 2010.
28. De Heer, M., Kapos, V. & Ten Brink, B. (2005) Biodiversity trends in Europe: development and testing of a species trend indicator for evaluating progress towards the 2010 target. Philosophical Transactions Royal Society London B, 360, 297-308.
29. De Snoo, G.R., Scheidegger, N.M.I. & de Jong, F.M.W. (1999) Vertebrate wildlife incidents with pesticides: a European survey. Pesticide Science, 55, 47-54.
30. Defra (2012a) https://secure.fera.defra.gov.uk/pusstats. Accessed 20/1/13
31. Defra (2012b) http://www.defra.gov.uk/statistics/foodfarm/food/cereals/cerealsoilseed/ Accessed 20/1/13.
32. DeLorenzo, M.E., Thompson, B., Cooper, E., Moore, J. & Fulton, M.H. (2012) A long-term monitoring study of chlorophyll, microbial contaminants, and pesticides in a coastal residential stormwater pond and its adjacent tidal creek. Environmental Monitoring and Assessment, 184, 343-359.
33. van Dijk, T.C. (2010). Effects of neonicotinoid pesticide pollution of Dutch surface water on non-target species abundance. MSc Thesis, Utrecht University, Utrecht.
34. Dively, G.P. & Kamel, A. (2012) Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. Journal of Agricultural and Food Chemistry, 60, 4449-4456.
35. Easton, A.H. & Goulson, D. (2013) The neonicotinoid insecticide imidacloprid repels pollinating flies and beetles at field-realistic levels. PLoS One, 8, e54819.
36. EFSA (2012) Statement on the findings in recent studies investigating sub-lethal effects in bees of some neonicotinoids in consideration of the uses currently authorised in Europe. EFSA Journal, 10, 2752.
37. EFSA (2013a) Conclusions on the peer review of the pesticide risk assessment for bees for the active substance clothianidin. EFSA Journal, 11, 3066.
38. EFSA (2013b) Conclusions on the peer review of the pesticide risk assessment for bees for the active substance thiamethoxam. EFSA Journal, 11, 3067.
39. EFSA (2013c) Conclusions on the peer review of the pesticide risk assessment for bees for the active substance imidacloprid. EFSA Journal, 11, 3068.
40. Fernández-Bayo, J.D., Nogales, R. & Romero, E. (2009) Effect of vermicomposts from wastes of the wine and alcohol industries in the persistence and distribution of imidacloprid and diuron on agricultural soils. Journal of Agricultural and Food Chemistry, 57, 5435-5442.
41. Flores-Céspedes, F., González-Pradas, E., Fernández-Pérez, M., Villafranca-Sánchez, M., Socías-Viciana, M. & Ureña-Amate, M.D. (2002) Effects of dissolved organic carbon on sorption and mobility of imidacloprid in soil. Journal of Environmental Quality, 3, 880-888.
42. Fox, R., Conrad, K.F., Parsons, M.S., Warren, M.S. & Woiwod, I.P. (2006). The State of Britain's Larger Moths. Butterfly Conservation and Rothamsted Research, Wareham, Dorset.
43. Gill, R.J., Ramos-Rodriguez, O. & Raine, N.E. (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature, 491, 105-119. doi: 10.1038/nature11585.
44. Goulson, D., Lye, G.C. & Darvill, B. (2008) Decline and conservation of bumblebees. Annual Review of Entomology, 53, 191-208.
45. Graham-Bryce, I.J. (1977) Crop protection: a consideration of the effectiveness and disadvantages of current methods and of the scope for improvement. Philosophical Transactions Royal Society London B, 281, 163-179.
46. Gregory, R.D., van Strien, A., Vorisek, P., Meyling, A.W.G., Noble, D.G., Foppen, R.P.B. et al. (2005) Developing indicators for European birds. Philosophical Transactions Royal Society London B, 360, 269-288.
47. Gupta, S., Gajbhiye, V.T. & Gupta, R.K. (2008) Soil dissipation and leaching behavior of a neonicotinoid insecticide thiamethoxam. Bulletin of Environmental Contamination and Toxicology, 80, 431-437.
48. Han, P., Niu, C.Y., Lei, C.L., Cui, J.J. & Desneux, N. (2010) Quantification of toxins in a Cry1Ac+CpTI cotton cultivar and its potential effects on the honey bee Apis mellifera L. Ecotoxicology, 19, 1612-1619.
49. Henry, M., Beguin, M., Requier, F., Rollin, O., Odoux, J.-F., Aupinel, P. et al. (2012) A common pesticide decreases foraging success and survival in honeybees. Science, 336, 350-351.
50. Horowitz, A., Kontsedalov, S. & Ishaaya, I. (2004) Dynamics of resistance to the neonicotinoids acetamiprid and thiamethoxam in Bemisia tabaci (Homoptera: Aleyrodidae). Journal of Economic Entomology, 97, 2051-2056.
51. Jeschke, P., Nauen, R., Schindler, M. & Elbert, A. (2011) Overview of the status and global strategy for neonicotinoids. Journal of Agricultural and Food Chemistry, 59, 2897-2908.
52. Johnson, K.D., O'Neal, M.E., Ragsdale, D.W., DiFonzo, C.D., Swinton, S.M., Dixon, P.M. et al. (2009) Probability of cost-effective management of soybean aphid (Hemiptera: Aphididae) in North America. Journal of Economic Entomology, 102, 2101-2108.
53. Kollmeyer, W.D., Flattum, R.F., Foster, J.P., Powell, J.E., Schroeder, M.E. & Soloway, S.B. (1999). Discovery of the nitromethylene heterocycle insecticides. Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor (eds I. Yamamoto & J. Casida ), pp. 71-89. Springer-Verlag, Tokyo.
54. Krupke, C.H., Hunt, G.J., Eitzer, B.D., Andino, G. & Given, K. (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One, 7, e29268.
55. Lamers, M., Anyusheva, M., La, N., Nguyen, V.V. & Streck, T. (2011) Pesticide pollution in surface and groundwater by paddy rice cultivation: a case study from Northern Vietnam. Clean-Soil Air Water, 39, 356-361.
56. Liukkonen-Anttila, T., Putaala, A. & Hissa, R. (1999) Does shifting from a commercial to a natural diet affect the nutritional status of hand-reared grey partridges Perdix perdix. Wildlife Biology, 5, 147-156.
57. Lopez-Antia, A., Ortiz-Santaliestra, M.E., Mougeot, F. & Mateo, R. (2013) Experimental exposure of red-legged partridges (Alectoris rufa) to seeds coated with imidacloprid, thiram and difenoconazole. Ecotoxicology, 22, 125-138.
58. Lye, G.C., Jennings, S.N., Osborne, J.L. & Goulson, D. (2011) Impacts of the use of nonnative commercial bumble bees for pollinator supplementation in raspberry. Journal of Economic Entomology, 104, 107-114.
59. Marzaro, M., Vivan, L., Targa, A., Mazzon, L., Mori, N., Greatti, M. et al. (2011) Lethal aerial powdering of honey bees with neonicotinoids from fragments of maize seed coat. Bulletin of Insectology, 64, 119-126.
60. McCornack, B.P. & Ragsdale, D.W. (2006) Efficacy of thiamethoxam to suppress soybean aphid populations in Minnesota soybean. Pest Management Network, doi:10.1094/CM-2006-0915-01-RS.
61. McKirdy, S.J., Jones, R.A.C. & Nutter Jr, F.W. (2002) Quantification of yield losses caused by Barley yellow dwarf virus in wheat and oats. Plant Diseases, 86, 769-773.
62. Metcalf, R.L. & Luckmann, W.H. (1994). Introduction to Insect Pest Management, pp. 266. New York: John Wiley and Sons, Inc.
63. Mommaerts, V., Reynders, S., Boulet, J., Besard, L., Sterk, G. & Smagghe, G. (2010) Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behaviour. Ecotoxicology, 19, 207-215.
64. Moritz, R.F.A., de Miranda, J., Fries, I., Le Cont, Y., Neumann, P. & Paxton, R.J. (2010) Research strategies to improve honeybee health in Europe. Apidologie, 41, 227-242.
65. Ohnesorg, W.J., Johnson, K.D. & O'Neal, M.E. (2009) Impact of reduced-risk insecticides on soybean aphid and associated natural enemies. Journal of Economic Entomology, 102, 1816-1826.
66. Oliver, J.B., Fare, D.C., Youssef, N., Scholl, S.S., Reding, M.E., Ranger, C.M. et al. (2010) Evaluation of a single application of neonicotinoid and multi-application contact insecticides for flatheaded borer management in field grown red maple cultivars. Journal of Environmental Horticulture, 28, 135-149.
67. Parry, M.A.J. & Hawkesford, M.J. (2010) Food security: increasing yield and improving resource use efficiency. Proceedings of the Nutrition Society, 69, 592-600.
68. Pena, A., Rodriguez-Liebana, J.A. & Mingorance, M.D. (2011) Persistence of two neonicotinoid insecticides in wastewater, and in aqueous solutions of surfactants and dissolved organic matter. Chemosphere, 84, 464-470.
69. Pollack, P. (2011). Fine Chemicals: The Industry and the Business, 2nd edn. John Wiley & Sons, New Jersey.
70. PPDB (2013) The Pesticide Properties Database (PPDB) developed by the Agriculture & Environment Research Unit (AERU). University of Hertfordshire, funded by UK national sources and the EU-funded FOOTPRINT project (FP6-SSP-022704). Available from: http://sitem.herts.ac.uk/aeru/projects/ppdb/index.htm Accessed 21/1/13
71. Rexrode, M., Barrett, M., Ellis, J., Gabe, P., Vaughan, A., Felkel, J. & Melendez, J. (2003). EFED Risk Assessment for the Seed Treatment of Clothianidin 600FS on Corn and Canola. United States Environmental Protection Agency, Washington, DC.
72. Royer, T.A., Giles, K.L., Nyamanzi, T., Hunger, R.M., Krenzer, E.G., Elliot, N.C., Kindler, S.D. & Payton, M. (2005) Economic evaluation of the effects of planting date and application rate of imidacloprid for management of cereal aphids and barley yellow dwarf in winter wheat. Journal of Economic Entomology, 98, 95-102.
73. Sarkar, M.A., Roy, S., Kole, R.K. & Chowdhury, A. (2001) Persistence and metabolism of imidacloprid in different soils of West Bengal. Pest Management Science, 57, 598-602.
74. Scorza, R.P., Smelt, J.H., Boesten, J.J.T.I., Hendriks, R.F.A. & van der Zee, S.E.A.T.M. (2004) Preferential flow of bromide, bentazon, and imidacloprid in a Dutch clay soil. Journal of Environmental Quality, 33, 1473-1486.
75. Seagraves, M.P. & Lundgren, J.G. (2012) Effects of neonicotinoid seed treatments on soybean aphid and its natural enemies. Journal of Pest Science, 85, 125-132.
76. Selim, H.M., Jeong, C.Y. & Elbana, T.A. (2010) Transport of imidacloprid in soils: miscible displacement experiments. Soil Science, 175, 375-381.
77. Starner, K. & Goh, K.S. (2012) Detection of the neonicotinoid insecticide imidacloprid in surface waters of three agricultural regions of California, USA, 2010-2011. Bulletin of Environmental Contamination and Toxicology, 88, 316-321.
78. Stoner, K.A. & Eitzer, B.D. (2012) Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS One, 7, e39114.
79. Suchail, S., Guez, D. & Belzunces, L.P. (2000) Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environmental Toxicology and Chemistry, 19, 1901-1905.
80. Sur, R. & Stork, A. (2003) Uptake, translocation and metabolism of imidacloprid in plants. Bulletin of Insectology, 56, 35-40.
81. Szendrei, Z., Grafius, E., Byrne, A. & Ziegler, A. (2012) Resistance to neonicotinoid insecticides in field populations of the Colorado potato beetle (Coleoptera: Chrysomelidae). Pest Management Science, 68, 941-946.
82. Tapparo, A., Marton, D., Giorio, C., Zanella, A., Solda, L., Marzaro, M. et al. (2012) Assessment of the environmental exposure of honeybees to particulate matter containing neonicotinoid insecticides coming from corn coated seeds. Environmental Science and Technology, 46, 2592-2599. doi: 10.1021/es2035152.
83. Thuyet, D.Q., Jorgenson, B.C., Wissel-Tyson, C., Watanabe, H. & Young, T.M. (2012) Wash off of imidacloprid and fipronil from turf and concrete surfaces using simulated rainfall. Science of the Total Environment, 414, 515-524.
84. Tomizawa, M. & Casida, J.E. (2005) Neonicotinoid insecticide toxicology: mechanisms of Selective Action. Annual Review of Pharmacology and Toxicology, 45, 247-268.
85. USEPA (2012) White Paper in Support of the Proposed Risk Assessment Process for Bees. Office of Chemical Safety and Pollution Prevention, United States Environmental protection Agency, Washington DC.
86. Van Dyck, H., Van Strien, A.J., Maes, D. & Van Swaay, C.A.M. (2009) Declines in common, widespread butterflies in a landscape under intense human use. Conservation Biology, 23, 957-965.
87. Whitehorn, P., O'Connor, S., Wackers, F. & Goulson, D. (2012) Neonicotinoid pesticide reduced bumble bee colony growth and queen production. Science, 336, 351-352.
88. Wilson, J.D., Evans, A.D. & Grice, P.V. (2010) Bird conservation and agriculture: a pivotal moment? Ibis, 152, 176-179.
89. Yang, E.C., Chuang, Y.C., Chen, Y.W. & Chang, H.C. (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology, 101, 1743-1748.
90. Yang, E.C., Chang, H.C., Wu, W.Y. & Chen, Y.W. (2012) Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS One, 7, e49472.