Imidacloprid effects on bees

Imidacloprid is a nicotine-derived systemic insecticide, belonging to a group of pesticides called neonicotinoids. Although it is off patent, the primary producer of imidacloprid is the German chemical firm Bayer CropScience. The trade names for imidacloprid include Gaucho, Admire, Merit, Advantage, Confidor, Provado, and Winner. Imidacloprid is a neurotoxin that is selectively toxic to insects relative to vertebrates and most non-insect invertebrates.[1] It acts as an agonist on the postsynaptic nicotinic acetylcholine receptors of motor neurones in insects. This interaction results in convulsions, paralysis, and eventually death of the poisoned insect.[2][3] It is effective on contact and via stomach action.[4] Because imidacloprid binds much more strongly to insect neuron receptors than to mammal neuron receptors, this insecticide is selectively more toxic to insects than mammals.[5] As a systemic pesticide, imidacloprid translocates or moves readily in the xylem of plants from the soil into the leaves, fruit, flowers, pollen, nectar, and guttation fluid of plants. Bees may be exposed to imidacloprid when they feed on the nectar, pollen, and guttation fluid of imidacloprid-treated plants.[6]

Experts believe that imidacloprid is one of many possible causes of bee decline and the recent bee malady termed colony collapse disorder (CCD). In 2011, according to the United States Department of Agriculture, no single factor alone is responsible for the malady, however honey bees are thought to possibly be affected by neonicotinoid chemicals existing as residues in the nectar and pollen which bees forage on. The scientists studying CCD have tested samples of pollen and have indicated findings of a broad range of substances, including insecticides, fungicides, and herbicides. They note that while the doses taken up by bees are not lethal, they are concerned about possible chronic problems caused by long-term exposure.[7][8]

In January 2013, the European Food Safety Authority stated that neonicotinoids pose an unacceptably high risk to bees, and that the industry-sponsored science upon which regulatory agencies' claims of safety have relied may be flawed, concluding that, "A high acute risk to honey bees was identified from exposure via dust drift for the seed treatment uses in maize, oilseed rape and cereals. A high acute risk was also identified from exposure via residues in nectar and/or pollen."[9] An author of a Science study prompting the EESA review suggested that industry science pertaining to neonicotinoids may have been deliberately deceptive, and the UK Parliament has asked manufacturer Bayer Cropscience to explain discrepancies in evidence they have submitted to an investigation.[10]

April 2013 the EU decided to restrict thiamethoxam and clothianidin along with imidacloprid.[11]

History

Regulatory and Usage History

Imidacloprid was first registered in the United Kingdom in 1993 and in the United States and France in 1994.[12] In the mid to late 1990s, French beekeepers reported a significant loss of bees, which they attributed to the use of imidacloprid. In 1999, the French Minister of Agriculture suspended the use of imidacloprid on sunflower seeds and appointed a team of expert scientists to examine the impact of imidacloprid on bees. In 2003, this panel, referred to as the Comité Scientifique et Technique (CST, or Scientific and Technical Committee) issued a 108-page report, which concluded that imidacloprid poses a significant risk to bees.[13] In 2004, the French Minister of Agriculture suspended the use of imidacloprid as a seed treatment for maize (corn). Despite these bans, colony collapse disorder still is occurring.[14]

Like most insecticides, imidacloprid is highly toxic to bees, with a contact acute LD50 = 0.078μg a.i./bee and an acute oral LD50 = 0.0039μg a.i./bee. Imidacloprid was first widely used in the United States in 1996 as it replaced 3 broad classes of insecticides. In 2006, U.S. commercial migratory beekeepers reported sharp declines in their honey bee colonies. This has happened in the past; however, unlike previous losses, adult bees were abandoning their hives. Scientists named this phenomenon colony collapse disorder (CCD). Reports show that beekeepers in most states have been affected by CCD.[7] Although no single factor has been identified as causing CCD, the United States Department of Agriculture (USDA), in their progress report on CCD, stated that CCD may be "a syndrome caused by many different factors, working in combination or synergistically."[15]

In a British parliamentary inquiry in 2012, the Environmental Audit Committee accused European regulators of ignoring evidence of imidacloprid risk to bees. The committee said that imidacloprid data available in the regulators' own assessment report shows "unequivocally that imidacloprid breaks down very slowly in soil, so that concentrations increase significantly year after year with repeated use, accumulating to concentrations very likely to cause mass mortality in most soil-dwelling animal life." The committee submitted a lengthy list of failings in current regulations including concerns that current regulations were set up for pesticide sprays, not systemic chemicals like imidacloprid that is used to treat seeds. They also expressed concern that only effects on honeybees have been considered despite the fact that 90% of pollination is carried out by different species, such as bumblebees, butterflies, moths and other insects. The environment minister responded saying that he is presently "...satisfied that the [European regulatory system] is working properly."[16]

Research History

Dave Goulson from the University of Stirling has found that trivial effects due to imidacloprid in lab and greenhouse experiments can translate into large effects in the field. The research found that bees consuming the pesticide suffered an 85% loss in the number of queens their nests produced, and a doubling of the number of bees who failed to return from food foraging trips.[17][18]

Researchers from the Harvard School of Public Health write that new research provides "convincing evidence" of the link between imidacloprid and the phenomenon known as Colony Collapse Disorder. Lead author of the study, Chensheng (Alex) Lu, stated that experiments showed a dose of 20 parts per billion of imidacloprid (less than the concentrations bees would encounter while foraging in sprayed crops), was enough to lead to Colony Collapse Disorder in 94% of colonies within 23 weeks.[19][20] The hives were nearly empty and the researchers did not find signs of the Nosema virus or Varroa mites.[21] The researchers proposed two possible sources of bees' exposure to imidacloprid. The first is through the nectar of plants sprayed with the pesticide itself, which is predicted by researchers at the University of Stirling, U.K., to have widespread impacts as imidacloprid is registered for use on over 140 crops in at least 120 countries.[18] The second is through the high-fructose corn-syrup that most bee-keepers in the United States use to feed their bees. Since application of imidacloprid to corn in the United States began in 2005 cases of Colony Collapse Disorder have grown significantly: from losses of 17% to 20% throughout the 1990s to somewhere between 30% and 90% of colonies in the United States since 2006.[7][22]

In May 2012, researchers at the University of San Diego released a study that showed that honey bees treated with a small dose of imidacloprid, comparable to what they would receive in nectar and formerly considered a safe amount, became "picky eaters," refusing nectars of lower sweetness and preferring to feed only on sweeter nectar. It was also found that bees exposed to imidacloprid performed the "waggle dance," the movements that bees use to inform hive mates of the location of foraging plants, at a lesser rate.[23]

Also in 2012, USDA researcher Jeff Pettis published the results of his study, which showed that bees treated with sub-lethal or low levels of imidacloprid had higher rates of infection with the pathogen Nosema than untreated bees.[24] His research confirmed that done by Alaux (2010) and Vidau (2011), who found that interactions between Nosema and neonicotinoids weakened bees and led to increased mortality.[25][26]

Toxicity of imidacloprid to bees

Acute

Imidacloprid is one of the most toxic insecticides to the western honeybee, Apis mellifera.[27] The toxicity of imidacloprid to Apis mellifera differs from most insecticides in that it is more toxic orally than by contact. The contact acute LD50 is 0.024 µg a.i./bee (micrograms of active ingredient per bee).[28] The acute oral LD50 ranges from 0.005 µg a.i./bee to 0.07 µg a.i./bee, which makes imidacloprid more toxic to the bees than the organophosphate dimethoate (oral LD50 0.152 µg/bee) or the pyrethroid cypermethrin (oral LD50 0.160 µg/bee).[27] Other insecticides that are equally or more toxic than imidacloprid include spinosad,[29] emamectin benzoate, fipronil, and the neonicotinoids clothianidin, thiamethoxam, and dinotefuran.[30]

Sublethal

The majority of studies that measure toxicity of pesticides to Apis mellifera honeybees focus on estimating the lethal dose (LD50) in acute toxicity tests to adult honeybees. This is only a partial measure of the harmful effects that pesticides can have on bees. For a complete analysis of the impact of pesticides to bees, sublethal effects should be considered.[31]

Dozens of research articles have been published in peer-reviewed journals, which show sublethal effects to adult bees exposed to low levels of imidacloprid.[31] In these studies, sub-lethal doses of 1-24μg/kg and 0.1 - 20 ng/bee have been shown to impair navigation, foraging behavior, feeding behavior, and olfactory learning performance in honeybees (Apis mellifera).[27][32][33][34][35][36][37][38] Other studies examining higher levels of imidacloprid (50 - 500 ppb) also found that imidacloprid decreases foraging activity and affects bee mobility and communication capacity.[39][40][41]

A 2012 in situ study sought to recreate hypothesized conditions of the initial outbreak of CCD in 2006/2007 by feeding honey bees high fructose corn syrup (HFCS) that the researchers laced with varying sub-lethal amounts of imidacloprid assumed to have been present in HFCS feed at the time. All but one of the colonies exposed to imidacloprid perished between 13 and 23 weeks post imidacloprid dosing, providing evidence that long-term sub-lethal exposure to the neonicotinoid causes honey bees to exhibit symptoms consistent with CCD months after exposure.[19]

Chronic

In 10-day chronic feeding studies with honeybees (Apis mellifera), 50% mortality was reached at levels between 0.1 and 10 ug/kg imidacloprid.[27] Other chronic toxicity studies conducted by Moncharmont et al. (2003) and Decourtye et al. (1999) have demonstrated chronic NOAEC values of <4 ppb and 4 ppb, respectively in honeybees.[42][43] In bumble bees, Mommaerts et al. (2009) demonstrated a LOAEC of 10 ppb for imidacloprid.[44]

Many tunnel and field studies have been conducted to show the potential effects of imidacloprid in the natural environment however most of these field studies have design and implementation deficiencies, which make them difficult to interpret and use.[13][30]

Synergistic effects

In 2012, researchers announced findings that sublethal exposure to imidacloprid rendered honey bees significantly more susceptible to infection by the fungus Nosema, thereby suggesting a potential link to CCD.[24] Two research teams led by Jeff Pettis at the U.S. Department of Agriculture and Cedric Alaux at INRA/France have demonstrated that interactions between the pathogen Nosema and imidacloprid significantly weaken the immune systems of honeybees (Apis mellifera). In their research, Alaux et al. (2010) found that bees infected with Nosema and exposed to 0.7 ug/kg imidacloprid had an increased rate of mortality compared to the controls. The combination of Nosema and imidacloprid also significantly decreased the activity of glucose oxidase, an important enzyme that allows the bees to sterilize their colony and brood food. Without this enzyme, bees can become more susceptible to infections by pathogens.[25] Both the USDA study and the INRA study demonstrate that a combination of stressors (pesticides and pathogens) may be responsible for the recent high level of bee losses.

Other studies

Bayer CropScience studies show that the maximum dose of imidacloprid for which no adverse effects were observed in bees is 20 ppb. Since Bayer claims that residue levels are usually below 5 ppb in pollen and nectar, they contend that imidacloprid poses a negligible risk to bees.[45]

Gerard Eyries, marketing manager for Bayer's agricultural division in France, states that studies confirm that imidacloprid leaves a small residue in nectar and pollen, but there is no evidence of a link with the drop in France's bee population, adding, "It is impossible to have zero residue. What is important is to know whether the very tiny quantities which have been found have a negative effect on bees." He also added that the product was sold in 70 countries with no reported side effects.[46]

Other independent studies have indicated that imidacloprid residues in plants can be higher:[13][47][48][49]

Uncertainties

It is important to note that the majority of studies conducted on pollinators have been performed in adult honeybees (Apis mellifera). Very few studies have been conducted on wild bees, most of which are solitary and raise their young in burrows and small colonies. There are also few studies that have been conducted on brood, larvae, or the queen, making it difficult to determine the impact of pesticides on different members of the colony and life stages of the bee. Although a number of field and semi-field studies have been conducted on imidacloprid and bees, these studies have design and implementation deficiencies, which make them unusable. Thus, the chronic effects of imidacloprid in the field are still unknown.[30]

Media portrayal

In October 2009, a documentary film, Vanishing of the Bees, was released in theatres in the UK. The film interviewed a number of experts in connection with CCD and suggested a link does exist between neonicotinoid pesticides and CCD. However, the experts interviewed conceded no firm scientific data yet exist. Industry-sponsored studies appear to be inconsistent with those produced by independent scientists. Until 2009 regulatory agencies still did not have conclusive data to determine the effects of imidacloprid on bee colonies.[13][50]

In February 2010, the documentary film Nicotine Bees was released. This film analyzes the possible factors contributing to the large bee die-offs worldwide and concludes that the large use of neonicotinoids is the most probable cause of the recent bee die-offs.[51]

See also

References

  1. ↑ http://www.fs.fed.us/foresthealth/pesticide/pdfs/122805_Imidacloprid.pdf
  2. ↑ Yamamoto, I.; Casida, J.E. (1999). Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor. Springer. ISBN 443170213X.
  3. ↑ Ishaaya, I. (2001). Biochemical Sites of Insecticide Action and Resistance. Springer. ISBN 3540676252.
  4. ↑ "Pesticide Information Profiles: Imidacloprid". Extension Toxicology Network. Retrieved April 7, 2012.
  5. ↑ Tomizawa, Motohiro (2004). "Neonicotinoids and Derivatives: Effects in Mammalian Cells and Mice". Journal of Pesticide Science. 29 (3): 177–183. doi:10.1584/jpestics.29.177. ISSN 1348-589X.
  6. ↑ Fossen, Matthew (2006). "Environmental Fate of Imidacloprid" (PDF). California Department of Pesticide Regulation. Retrieved 18 April 2012.
  7. 1 2 3 Johnson, Renée (7 January 2010). "Honey Bee Colony Collapse Disorder". Congressional Research Service. Retrieved 18 April 2012.
  8. ↑ Decourtye, Axel; Devillers, James (2010). "Ecotoxicity of Neonicotinoid Insecticides to Bees". In Thany, Steeve Hervé. Insect Nicotinic Acetylcholine Receptors (Advances in Experimental Medicine and Biology). 683. pp. 85–95. doi:10.1007/978-1-4419-6445-8_8. ISBN 978-1-4419-6444-1.
  9. ↑ European Food Safety Authority (16 January 2013) "Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin" EFSA Journal 11(1):3066.
  10. ↑ Damian Carrington (16 January 2013) "Insecticide 'unacceptable' danger to bees, report finds" The Guardian
  11. ↑ EU to Restrict 'Bee-Harming' Pesticides April 29, 2013 Wall Street Journal
  12. ↑ Pesticide Action Network. Imidacloprid
  13. 1 2 3 4 Comité Scientifique et Technique (18 September 2003). "Imidaclopride utilisé en enrobage de semences (Gaucho) et troubles des abeilles: Rapport final" [Imidacloprid used in coating seeds (Gaucho) and disorders of bees: Final report] (PDF) (in French). Retrieved 18 April 2012.
  14. ↑ [European Draft Assessment Report: Imidacloprid. Annex B, B.7. February 2006]
  15. ↑ "USDA Colony Collapse Disorder Progress Report" (PDF). USDA Agriculture Research Service. June 2010. Retrieved April 7, 2012.
  16. ↑ Carrington, Damian (12 December 2012). "Insecticide regulators ignoring risk to bees, say MPs". The Guardian. London.
  17. ↑ Carrington, Damian (March 29, 2012). "Pesticides linked to honeybee decline". London: The Guardian. Retrieved April 7, 2012.
  18. 1 2 Whitehorn, P. R.; O'Connor, S.; Wackers, F. L.; Goulson, D. (2012). "Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth and Queen Production". Science. 336 (6079): 351–2. doi:10.1126/science.1215025. ISSN 0036-8075. PMID 22461500.
  19. 1 2 Lu, Chensheng; Warchol, K. M.; Callahan, R. A. (2012). "In situ replication of honey bee colony collapse disorder (13 March 2012 corrected proof)" (PDF). Bulletin of Insectology. 65 (1). ISSN 1721-8861. Retrieved 7 April 2012.
  20. ↑ Datz, Todd (5 April 2012). "Press Release: Use of Common Pesticide Linked to Bee Colony Collapse". Harvard School of Public Health. Retrieved 18 April 2012.
  21. ↑ Harmon, Katherine. "Common Pesticide Implicated Bee Colony Collapse Disorder". Scientific American blog. Retrieved 15 April 2012.
  22. ↑ Tapparo, A.; Marton, D.; Giorio, C.; Zanella, A.; Soldà, L.; Marzaro, M.; Vivan, L.; Girolami, V. (2012). "Assessment of the Environmental Exposure of Honeybees to Particulate Matter Containing Neonicotinoid Insecticides Coming from Corn Coated Seeds". Environmental Science & Technology. 46 (5): 2592–2599. doi:10.1021/es2035152. PMID 22292570.
  23. ↑ Commonly Used Pesticide Turns Honey Bees into ‘Picky Eaters’
  24. 1 2 Pettis, Jeffery S.; vanEngelsdorp, Dennis; Johnson, Josephine; Dively, Galen (2012). "Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema". Naturwissenschaften. 99 (2): 153–158. doi:10.1007/s00114-011-0881-1. ISSN 0028-1042. PMC 3264871Freely accessible. PMID 22246149.
  25. 1 2 Alaux, Cédric; Brunet, Jean-Luc; Dussaubat, Claudia; Mondet, Fanny; Tchamitchan, Sylvie; Cousin, Marianne; Brillard, Julien; Baldy, Aurelie; Belzunces, Luc P.; Le Conte, Yves (2010). "Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera)". Environmental Microbiology. 12 (3): 774–782. doi:10.1111/j.1462-2920.2009.02123.x. ISSN 1462-2912. PMC 2847190Freely accessible. PMID 20050872.
  26. ↑ Didier, Elizabeth; Vidau, Cyril; Diogon, Marie; Aufauvre, Julie; Fontbonne, Régis; Viguès, Bernard; Brunet, Jean-Luc; Texier, Catherine; Biron, David G.; Blot, Nicolas; El Alaoui, Hicham; Belzunces, Luc P.; Delbac, Frédéric (2011). "Exposure to Sublethal Doses of Fipronil and Thiacloprid Highly Increases Mortality of Honeybees Previously Infected by Nosema ceranae". PLoS ONE. 6 (6): e21550. doi:10.1371/journal.pone.0021550. ISSN 1932-6203. PMC 3125288Freely accessible. PMID 21738706.
  27. 1 2 3 4 Suchail, Séverine; Guez, David; Belzunces, Luc P. (2001). "Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera". Environmental Toxicology and Chemistry. 20 (11): 2482–2486. doi:10.1002/etc.5620201113. PMID 11699773.
  28. ↑ Suchail, Séverine; Guez, David; Belzunces, Luc P. (July 2000). "Characteristics of imidacloprid toxicity in two Apis mellifera subspecies". Environmental Toxicology and Chemistry. 19: 1901–1905. doi:10.1002/etc.5620190726.
  29. ↑ Biondi, Antonio; Mommaerts Veerle; Smagghe Guy; Vinuela Elisa; Zappalà Lucia; Desneux Nicolas (2012). "The non-target impact of spinosyns on beneficial arthropods". Pest Management Science. 68: 1523–1536. doi:10.1002/ps.3396.
  30. 1 2 3 Federoff, N.E.; Vaughan, Allen; Barrett, M.R. (13 November 2008). "Environmental Fate and Effects Division Problem Formulation for the Registration Review of Imidacloprid". US EPA. Retrieved 18 April 2012.
  31. 1 2 Desneux, Nicolas; Decourtye Axel; Delpuech Jean-Marie (2007). "The sublethal effects of pesticides on beneficial arthropods". Annual Review of Entomology. 52: 81–106. doi:10.1146/annurev.ento.52.110405.091440.
  32. ↑ Armengaud, C.; Lambin, M.; Gauthier, M. (2002), "Effects of imidacloprid on the neural processes of memory", in Devillers, J; Pham-Delegue, M.H., Honey bees: estimating the environmental impact of chemicals, New York: Taylor & Francis, pp. 85–100, ISBN 9780415275187
  33. ↑ Decourtye, A; Lacassie, E; Pham-Delegue, M-H (2003). "Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season". Pest Manage Sci. 59: 269–278. doi:10.1002/ps.631.
  34. ↑ Decourtye, A.; Armengaud, C.; Devillers, R.M.; Cluzeau, S. (2004). "Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L)". Pesticide Biochem Phys. 78: 83–92. doi:10.1016/j.pestbp.2003.10.001.
  35. ↑ Guez, D.; Suchail, S.; Gauthier, M.; Maleszka, R.; Belzunces, L. (2001). "Contrasting effects of imidacloprid on habituation in 7- and 8-day old honeybees (Apis mellifera)". Neurobiol Learning Memory. 76: 183–191. doi:10.1006/nlme.2000.3995.
  36. ↑ Pham-Delegue, M.H.; Cluzeau, S. (1999), "Effets des produits phytosanitaires sur l'abeille; incidence du traitement des semences de tournesol par Gaucho sur les disparitions de butineuses", Rapport final de synthese au Ministere de l’Agriculture et de la Peche
  37. ↑ Lambin, M.; Armengaud, C.; Ramond, S.; Gauthier, M. (2001). "Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee". Arch Insect Biochem Physiol. 48: 129–134. doi:10.1002/arch.1065.
  38. ↑ Williamson, S.M.; Wright, G.A (2013). "Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees" (PDF). Journal of Experimental Biology. 216 (10): 1799–1807. doi:10.1242/jeb.083931. ISSN 0022-0949. PMC 3641805Freely accessible. PMID 23393272.
  39. ↑ Medrzycki, P.; Montanari, R.; Bortolotti, L.; Sabatini, A. G.; Maini, S.; Porrini, C. (2003). "Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests" (PDF). Bulletin of Insectology. 56 (1): 59–62. ISSN 1721-8861.
  40. ↑ Yang, E.C.; Chuang, Y.C.; Chen, Y.L.; Chang, L.H (2008). "Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honeybee (Hymenoptera: Apidae)". J. Econ Entomology. 101 (6): 1743–1748. doi:10.1603/0022-0493-101.6.1743.
  41. ↑ Bortolotti, L.; Montanari R.; Marcelino J.; Medrzycki P.; Maini S.; Porrini C. (2003). "Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees" (PDF). Bulletin of Insectology. 56 (1): 63–67. ISSN 1721-8861.
  42. ↑ Moncharmont, F.D.; Decourtye, A.; Hantier, C.H.; Pons, O.; Pham-Delegue, M. (2003). "Statistical analysis of honeybee survival after chronic exposure to insecticides". Environ Toxicol Chem. 22 (12): 3088–94. doi:10.1897/02-578.
  43. ↑ Decourtye, A.; Metayer, M., Pottiau, H., Tisseur, M., Odoux, J.F., Pham-Delegue, M.H. (1999), "Impairment of olfactory learning performances in the honeybee after long-term ingestion of imidacloprid", Hazards of Pesticides to Bees, Paris: INRA
  44. ↑ Mommaerts, V.; Reynders, S.; Boulet, J.; Besard, L.; Sterk, G.; Smagghe, G. (2009). "Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior". Ecotoxicology. 19: 207–215. doi:10.1007/s10646-009-0406-2.
  45. ↑ Maus, C.; Curé, G.; Schmuck, R. (2003). "Safety of imidacloprid seed dressings to honey bees: a comprehensive overview and compilation of the current state of knowledge" (PDF). Bulletin of Insectology. 56 (1): 51–57. ISSN 1721-8861.
  46. ↑ French honey makers in a buzz over pesticides
  47. ↑ Bonmatin, J.M.; Marchand, P.A.; Charvet, R.; Moineau, I.; Bengsch, E.R.; Colin, M.A. (2005). "Quantification of imidacloprid uptake in maize crops". J. Agric. Food Chem. 53 (13): 5336–5341. doi:10.1021/jf0479362. PMID 15969515.
  48. ↑ Laurent, F.M.; Rathahao, E. (2003). "Distribution of 14C-imidacloprid in sunflowers (Helianthus annuus L.) following seed treatment". J Agric Food Chem. 51 (27): 8005–10. doi:10.1021/jf034310n.
  49. ↑ http://www.millersriver.net/pollen/talks/Microsoft%20PowerPoint%20-%20Kim%20Stoner%20pdf%20for%20posting.pdf Archived June 27, 2011, at the Wayback Machine.
  50. ↑ Official website of the 2009 documentary Vanishing of the Bees
  51. ↑ Nicotine Bees website
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