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Neonicotinoids

Neonicotinoids are now the most widely used insecticides in the world and the most studied class of insecticides for bees [1]. They were developed in the 1990s in response to pest resistance and can target several pests in the Homoptera, Coleoptera, and Lepidoptera family [2, 3]. They are also less toxic to vertebrates than common older insecticides due to their increased selectivity to insect acetylcholine receptors in the brain [3].  These benefits have led to their widespread use in agriculture and residential areas; however, they have been under scrutiny due to their persistence in the soil, ability to leach into the environment, high water solubility, and potential negative health implications for non-target organisms such as pollinators [4]. The contradictory findings for the effects of neonicotinoids on honey bees has caused them to be a very controversial topic for policy decisions.

This section only provides a brief overview of the scientific evidence. For more detailed information please read the following reviews or the individual articles cited in this section:

[5] Decourtye, A. and J. Devillers (2010). Ecotoxicity of Neonicotinoid Insecticides to Bees. Insect Nicotinic Acetylcholine Receptors. S. H. Thany. (editor). 683: 85-95.

[4] The Task Force on Systemic Pesticides (2015). Worldwide integrated assessment on systemic pesticides. Environmental Science and Pollution Research 22: 1-305.

[6] Blacquière, T., et al. (2012). "Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment." Ecotoxicology 21(4): 973-992. 

[1] Lundin, O., et al. (2015). "Neonicotinoid insecticides and their impacts on bees: a systematic review of research approaches and identification of knowledge gaps." Plos One 10(8): e0136928.

Neonicotinoids are used in over 120 countries and have 140 different crop uses [1]. They can be sprayed onto foliage or applied as soil drenches, but they are predominantly used as seed treatments. When used this way, neonicotinoids are taken up by all parts of the plant as it grows. This means these systemic insecticides are present in pollen and nectar that pollinators can come in contact with when foraging. In addition, they have been found on neighboring flowers and grass [7, 8] (even at levels higher than the crops they were applied to [9]), in nearby waterways [10], and they persist in the soil for long periods of time [11]. The ability for these insecticides to escape into the environment and affect non-target organisms has sparked a lot of research interest into evaluating their implications and risks [4].

There are 8 neonicotinoids that are commercially available: imidacloprid, thiacloprid, clothianidin, thiamethoxam, acetamiprid, nitenpyram, dinotefuran, and sulfoxaflor (although the approval of this last neonic, sulfloxaflor, has recently been cancelled by the EPA due to flawed and limited data [12]). There is variation in the effect of these different neonicotinoids based on their chemical structure. Nitro-containing neonicotinoids (imidacloprid, thiamethoxam, clothianidin) are generally more toxic to bees than cyano-containing neonicotinoids (acetamiprid and thiacloprid). Overall, neonicotinoids are emerging as being more toxic than other pesticides to bees. For instance, Sanchez-Bayo and Goka [13] assessed the risk of 92 individual compounds (insecticides, fungicides, miticides, herbicides) and 3 neonicotinoids comprised the top five chemicals that are considered the highest risk to honey bees and bumble bees.

Overall, the majority of laboratory and semi-field research demonstrates neonicotinoids can be harmful to honey bees; however, the majority of field studies find only limited or no effects on honey bees. It is here that the controversy lies. The most convincing evidence for the effect of these pesticides come from large-scale field studies that investigate the real world effects of bees pollinating our agricultural systems. Of these types of studies accomplished to date with the honey bee (nine in total) [14-22], only four report at least some negative consequences [19-22].

The impact of neonicotinoids on bumble bees is more in agreement. The majority of lab, semi field, and field studies report negative implications of neonicotinoids. Of four field studies investigating bumble bees [23-26], three report such effects [23, 25, 26]. These bees are about 2-3 times more sensitive than honey bees to neonicotinoid toxicity [13, 27, 28]. Neonicotinoids also cause more lethal and sublethal effects on bumble bees compared to other pesticides [29].

 Lab Studies

Laboratory studies investigating honey bees find neonicotinoids are associated with the following outcomes:

  • Increased mortality [articles in support: 30, 31-39] [articles in disagreement: 34, 40, 41, 42]
  • Impaired feeding [articles in support: 43, 44] [articles in disagreement: 28]),
  • Impaired locomotion [articles in support: 44, 45, 46, 47] [articles in disagreement: 28, 40]
  • Altered learning and memory [articles in support: 47, 48, 49, 50] [articles in disagreement: 40, 51]
  • Impaired foraging [articles in support: 43]
  • Reduced immunity [articles in support: 40, 51]

Lab studies also find neonicotinoids affect bumble bees in the following ways:

  • Increased mortality [52, 53]
  • Reduced colony growth [29, 54-56]
  • Reduced brood production [57, 58]
  • Reduced nest construction [29, 54, 58-61]
  • Impaired feeding [articles in support: 28, 29, 47, 61, 62] [articles in disagreement: 54]
  • There is contradicting evidence for the effect on locomotion [47] and longevity [28, 47]

Laboratory studies examining wild bees report the following impacts:

  • Mortality [38, 63-65]
  • Reduced brood production [63]
  • Altered locomotion [64]

In addition to these impacts, honey bees and bumble bees will preferentially choose drink sucrose solution spiked with neonicotinoids compared to solution without [54]. Taken together, these studies demonstrate that in laboratory conditions, neonicotinoids can be harmful to bees. They evaluate how neonicotinoids cause impairments at the individual level. These studies do not represent neonicotinoid exposure in normal agricultural settings. Honey bees and bumble bees are social animals found in colonies, and they forage on a variety of plant sources. There could be buffered effects from being in a colony environment and from the presence of other pollen and nectar types that are not taken into account through laboratory studies.

Field Studies

Semi field studies have a more realistic element to them. Bees are able to forage outside and are found in colony environments. In semi-field studies, researchers are still manipulating pesticide exposure to bees. Usually they supplement bees with protein patties or sugar syrups containing neonicotinoids and place the colonies out in a field.

Semi-field studies on honey bees show that neonicotinoids are associated with the following outcomes:

  • Altered foraging behavior [articles in support: 50, 66, 67-71] [articles in disagreement: 39, 72]
  • Increased mortality [articles in support: 73, 74] [articles in disagreement: 39]
  • Reduced colony growth [67]
  • Reduced feeding [66]
  • Impaired learning and memory [50]
  • Queen problems [67, 75]
  • Reduced honey production [67]
  • Increased infection [76].
  • There are conflicting reports of overwintering effects [67, 77]

Semi-field studies on honey bees have also investigated effects on brood production, locomotion, longevity, and comb building [39, 72], but none have found negative implications associated with neonicotinoids. Overall, many semi-field studies report negative impacts of neonicotinoids on honey bee health at the individual and colony level.

There have been ten field studies examining honey bee health during and following exposure to neonicotinoids. Only two studies have found effects on mortality [19, 22], while several others have found no effect [14-18, 78]. There are conflicting reports on the outcomes on foraging behavior [17, 19]. There are no reported effects on colony growth [14-17, 22, 78], brood production [15-17, 22, 78], honey production [14, 16, 17, 22, 78], or overwintering success [17, 78, 79]. However, studies have documented changes in acetylcholinesterase activity [20, 21] and increases in pathogen infection [20]. Overall, the majority of studies do not find impacts at the colony level, but do observe impacts at the individual and sub-individual level.

Semi field studies with bumble bees continue to document negative outcomes from neonicotinoid exposure. The following outcomes are affected:

  • Foraging [articles in support: 80, 81-83] [articles in disagreement: 84]
  • colony growth [85, 86]
  • queen production [85, 86]
  • brood production [87]
  • locomotion [80]
  • Mortality [articles in support: 80] [articles in disagreement: 84]

Field studies have also found implications with brood production [24, 26] and queen production [24, 25]. Some studies find negative impacts on colony growth [24, 25], while others do not [23]. Furthermore, one study reported no impacts on foraging or homing behavior when examining these outcomes [23].

Reconciliation between lab and field discrepancies in honey bees

The discrepancy between laboratory and field studies is beginning to be uncovered. A large-scale field study in France found that field exposure to neonicotinoids is associated with increased individual mortality [22]. However, colonies are able to buffer against this loss so that there are no detectable changes in performance (e.g., brood production and honey production). Specifically, the study suggests colonies invest less energy into drone production (which is energetically costly) so that they can maintain honey and worker production.

Interaction Effects

Neonicotinoid-pesticide

Interaction effects between neonicotinoids and pyrethroids have been documented in semi-field studies on bumble bees [87]. This combination can lead to impaired foraging, increased worker mortality, and increased colony failure. The toxicity of neonicotinoids is also increased when found in combination with fungicides. For instance, thiacloprid is more toxic when combined with fungicides in the lab, but this effect is not seen in semi-field trials [13, 88]. Negative effects from combinations of imidacloprid with thiacloprid have been documented in both honey bees and managed Osmia cornifrons [30] as well.

Neonicotinoid-disease

There have been documentations of neonicotinoids interactions with gut parasites in bumble bees. Exposure of neonicotinoids and Crithidia bombii combined lead to increased queen mortality [58].

References

  1. Lundin, O., et al., 2015. Neonicotinoid insecticides and their impacts on bees: a systematic review of research approaches and identification of knowledge gaps. PLoS One,  10(8): p. e0136928.
  2. Jeschke P, N.R., Schindler M, Elbert A, 2011. Overview of the status and global strategy for neonicotinoids. J Agric Food Chem,  59: p. 2897–2908.
  3. Jeschke P, N.R., 2008. Neonicotinoids—from zero to hero in insecticide chemistry. Pest Manag Sci,  64: p. 1084–1098.
  4. The Task Force on Systemic Pesticides, 2015. Worldwide integrated assessment on systemic pesticides. Environmental Science and Pollution Research,  22: p. 1-305.
  5. Decourtye, A. and J. Devillers, 2010. Ecotoxicity of Neonicotinoid Insecticides to Bees, in Insect Nicotinic Acetylcholine Receptors, S.H. Thany, Editor. p. 85-95.
  6. Blacquière, T., et al., 2012. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology,  21(4): p. 973-992.
  7. Greatti, M., et al., 2006. Presence of the a.i. imidacloprid on vegetation near corn fields sown with Gaucho((R)) dressed seeds. Bulletin of Insectology,  59(2): p. 99-103.
  8. Krupke, C.H., et al., 2012. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One,  7: p. e29268.
  9. Botías, C., et al., 2015. Neonicotinoid residues in wildflowers, a potential route of chronic exposure for bees. Environmental Science & Technology,  49: p. 12731−12740.
  10. Tišler T, J.A., Mozetic B, Trebse P, 2009. Hazard identification of imidacloprid to aquatic environment. Chemosphere,  76: p. 907-914.
  11. Jones, A., P. Harrington, and G. Turnbull, 2014. Neonicotinoid concentrations in arable soils after seed treatment applications in preceding years. Pest Management Science,  70(12): p. 1780-1784.
  12. Environmental Protection Agency, Sulfloxaflor - Final Cancellation Order. 2015.
  13. Sanchez-Bayo, F. and K. Goka, 2014. Pesticide Residues and Bees - A Risk Assessment. Plos One,  9(4).
  14. Cutler, G.C., et al., 2014. A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. PeerJ,  2: p. e652.
  15. Pohorecka, K., et al., 2013. EFFECTS OF EXPOSURE OF HONEY BEE COLONIES TO NEONICOTINOID SEED-TREATED MAIZE CROPS. Journal of Apicultural Science,  57(2): p. 199-208.
  16. Pohorecka, K., et al., 2012. RESIDUES OF NEONICOTINOID INSECTICIDES IN BEE COLLECTED PLANT MATERIALS FROM OILSEED RAPE CROPS AND THEIR EFFECT ON BEE COLONIES. Journal of Apicultural Science,  56(2): p. 115-134.
  17. Pilling, E., et al., 2013. 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: p. e77193.
  18. Nguyen, B.K., et al., 2009. Does imidacloprid seed-treated maize have an impact on honey bee mortality? Journal of Economic Entomology,  102: p. 616-623.
  19. Tremolada, P., et al., 2010. Field Trial for Evaluating the Effects on Honeybees of Corn Sown Using Cruiser(A (R)) and Celest xl(A (R)) Treated Seeds. Bulletin of Environmental Contamination and Toxicology,  85(3): p. 229-234.
  20. Alburaki, M., et al., 2015. Neonicotinoid-Coated Zea mays Seeds Indirectly Affect Honeybee Performance and Pathogen Susceptibility in Field Trials. Plos One,  10(5).
  21. Boily, M., et al., 2013. Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids, atrazine and glyphosate: laboratory and field experiments. Environmental Science and Pollution Research,  20(8): p. 5603-5614.
  22. Mickaël Henry, N.C., Pierrick Aupinel, Axel Decourtye, Mélanie Gayrard, Jean-François Odoux, Aurélien Pissard, Charlotte Rüger, Vincent Bretagnolle, 2015. Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees. Proceedings of the Royal Society B-Biological Sciences,  282: p. 20152110.
  23. Tasei, J.N., G. Ripault, and E. Rivault, 2001. Hazards of imidacloprid seed coating to Bombus terrestris (Hymenoptera : Apidae) when applied to sunflower. Journal of Economic Entomology,  94(3): p. 623-627.
  24. Rundlöf, M., G. K. S. Andersson, R. Bommarco, I. Fries, V. Hederström, L. Herbertsson, O. Jonsson, B. K. Klatt, T. R. Pedersen, J. Yourstone and H. G. Smith 2015. Seed coating with a neonicotinoid insecticide negatively impacts wild bees. Nature,  521: p. 77-80.
  25. Goulson, D., 2015. Neonicotinoids impact bumblebee colony fitness in the field; a reanalysis of the UK’s food & environment research agency 2012 experiment. PeerJ,  3: p. e854.
  26. Cutler, G.C. and C.D. Scott-Dupree, 2014. A field study examining the effects of exposure to neonicotinoid seed-treated corn on commercial bumble bee colonies. Ecotoxicology,  23: p. 1755-1763.
  27. Cresswell, J.E., et al., 2014. Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris). Pest Management Science,  70(2): p. 332-337.
  28. Cresswell, J.E., et al., 2012. Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology,  115: p. 365-371.
  29. Gradish, A.E., et al., 2010. Effect of reduced risk pesticides for use in greenhouse vegetable production on Bombus impatiens (Hymenoptera: Apidae). Pest Management Science,  66: p. 142-146.
  30. Biddinger, D.J., et al., 2013. Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS One,  8(9): p. e72587.
  31. Suchail, S., D. Guez, and L.P. Belzunces, 2001. Toxicity of imidacloprid and its metabolites in Apis mellifera, in Hazards of Pesticides to Bees, L.P. Belzunces, C. Pelissier, and G.B. Lewis, Editors. p. 121-126.
  32. Iwasa, T., et al., 2004. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection,  23(5): p. 371-378.
  33. Marzaro, M., et al., 2011. Lethal aerial powdering of honey bees with neonicotinoids from fragments of maize seed coat. Bulletin of Insectology,  64(1): p. 119-126.
  34. Laurino, D., et al., 2011. Toxicity of neonicotinoid insecticides to honey bees: laboratory tests.Bulletin of Insectology,  64(1): p. 107-113.
  35. Moncharmont, F.X.D., et al., 2003. Statistical analysis of honeybee survival after chronic exposure to insecticides. Environmental Toxicology and Chemistry,  22(12): p. 3088-3094.
  36. Decourtye, A., E. Lacassie, and M.H. Pham-Delegue, 2003. Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Management Science,  59(3): p. 269-278.
  37. Suchail, S., D. Guez, and L.P. Belzunces, 2000. Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environmental Toxicology and Chemistry,  19(7): p. 1901-1905.
  38. Scott-Dupree, C.D., L. Conroy, and C.R. Harris, 2009. Impact of currently used or potentially useful insecticides for canola agroecosystems on Bombus impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymentoptera: Megachilidae), and Osmia lignaria (Hymenoptera: Megachilidae). Journal of Economic Entomology,  102: p. 177-182.
  39. Schmuck, R., et al., 2001. Risk posed to honeybees (Apis mellifera L. Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Management Science,  57(3): p. 225-238.
  40. Aliouane Y, E.H.A., Gary V, Armengaud C, Lambin M, Gauthier M, 2009. Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior. Environ Toxicol Chem,  28(1): p. 113-122.
  41. Bailey, J., et al., 2005. Contact and oral toxicity to honey bees (Apis mellifera) of agents registered for use for sweet corn insect control in Ontario, Canada. Apidologie,  36: p. 623-633.
  42. Schmuck, R., 2004. Effects of a chronic dietary exposure of the honeybee Apis mellifera (Hymenoptera : Apidae) to imidacloprid. Archives of Environmental Contamination and Toxicology,  47(4): p. 471-478.
  43. Ramirez-Romero, R., J. Chaufaux, and M.H. Pham-Delegue, 2005. Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie,  36(4): p. 601-611.
  44. Lambin, M., et al., 2001. Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. Archives of Insect Biochemistry and Physiology,  48(3): p. 129-134.
  45. Teeters, B.S., et al., 2012. Using video-tracking to assess sublethal effects of pesticides on honey bees (Apis mellifera L.). Environmental Toxicology and Chemistry,  31(6): p. 1349-1354.
  46. Williamson, S.M., S.J. Willis, and G.A. Wright, 2014. Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology,  23: p. 1409-1418.Kessler, S.C., E. J. Tiedeken, K. L. Simcock, S. Derveau, J. Mitchell, S. S., J. C. Stout and G. A. Wright 2015. Bees prefer foods containing neonicotinoid pesticides. Nature,  521: p. 74-76.
  47. Han, P., et al., 2010. Use of an innovative T-tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera L. Ecotoxicology,  19(8): p. 1612-1619.
  48. El Hassani, A.K., et al., 2008. Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Archives of Environmental Contamination and Toxicology,  54(4): p. 653-661.
  49. Decourtye, A., et al., 2004. Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicology and Environmental Safety,  57(3): p. 410-419.
  50. 51.       Williamson, S.M., D.D. Baker, and G.A. Wright, 2013. Acute exposure to a sublethal dose of imidacloprid and coumaphos enhances olfactory learning and memory in the honeybee Apis mellifera. Invertebrate Neuroscience,  13(1): p. 63-70.
  51. 52.       Di Prisco, G., et al., 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences of the United States of America,  110(46): p. 18466-18471.
  52. 53.       Vidau, C., et al., 2011. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. Plos One,  6: p. e21550.
  53. 54.       Tasei, J.N., J. Lerin, and G. Ripault, 2000. Sub-lethal effects of imidacloprid on bumblebees, Bombus terrestris (Hymenoptera: Apidae), during a laboratory feeding test. Pest Management Science,  56: p. 784-788.
  54. 55.       Marletto, F., A. Patetta, and A. Manino, 2003. Laboratory assessment of pesticide toxicity to bumblebees. Bulletin of Insectology,  56(1): p. 155-158.
  55. 56.       Scott-Dupree, C.D., L. Conroy, and C.R. Harris, 2009. Impact of currently used or potentially useful insecticides for canola agroecosystems on Bombus impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymenoptera: Megachilidae), and Osmia lignaria (Hymenoptera: Megachilidae).Journal of Economic Entomology,  102: p. 177-182.
  56. 57.       Bryden, J., et al., 2013. Chronic sublethal stress causes bee colony failure. Ecology Letters,  16: p. 1463-1469.
  57. 58.       Fauser-Misslin, A., et al., 2014. Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory. Journal of Applied Ecology,  51(2): p. 450-459.
  58. 59.       Laycock, I., et al., 2012. Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology,  21: p. 1937-1945.
  59. 60.       Laycock, I., et al., 2014. Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on microcolonies of Bombus terrestris worker bumble bees. Ecotoxicology and Environmental Safety,  100: p. 153-158.
  60. 61.       Laycock, I. and J.E. Cresswell, 2013. Repression and recuperation of brood production in Bombus terrestris bumble bees exposed to a pulse of the neonicotinoid pesticide imidacloprid. PloS One,  8: p. e79872.
  61. 62.       Elston, C., H.M. Thompson, and K.F.A. Walters, 2013. Sub-lethal effects of thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (Bombus terrestris) micro-colonies. Apidologie,  44: p. 563-574.
  62. Sandrock, C., et al., 2014. Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agricultural and Forest Entomology,  16: p. 119-128.
  63. Tome, H.V.V., et al., 2012. Imidacloprid-Induced Impairment of Mushroom Bodies and Behavior of the Native Stingless Bee Melipona quadrifasciata anthidioides. Plos One,  7(6).
  64. Valvovinos-Nunez, G.R., et al., 2009. Comparative Toxicity of Pesticides to Stingless Bees (Hymenoptera: Apidae: Meliponini). Journal of Economic Entomology,  102(5): p. 1737-1742.
  65. Eiri, D.M. and J.C. Nieh, 2012. A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. Journal of Experimental Biology,  215(12): p. 2022-2029.
  66. Sandrock, C., et al., 2014. Impact of Chronic Neonicotinoid Exposure on Honeybee Colony Performance and Queen Supersedure. Plos One,  9(8).
  67. Schneider, C.W., et al., 2012. RFID Tracking of Sublethal Effects of Two Neonicotinoid Insecticides on the Foraging Behavior of Apis mellifera. Plos One,  7(1).
  68. Yang, E.C., et al., 2008. Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol,  101: p. 1743-1748.
  69. Fischer, J., et al., 2014. Neonicotinoids interfere with specific components of navigation in honeybees. PLoS One,  9: p. e91364.
  70. Henry, M., et al., 2012. A common pesticide decreases foraging success and survival in honey bees. Science,  336: p. 348-350.
  71. Faucon, J.P., et al., 2005. Experimental study on the toxicity of imidacloprid given in syrup to honey bee (Apis mellifera) colonies. Pest Management Science,  61(2): p. 111-125.
  72. Lu, C.S., K.M. Warchol, and R.A. Callahan, 2012. In situ replication of honey bee colony collapse disorder. Bulletin of Insectology,  65(1): p. 99-106.
  73. Sgolastra, F., et al., 2012. Effects of neonicotinoid dust from maize seed-dressing on honey bees. Bulletin of Insectology,  65(2): p. 273-280.
  74. Williams, G.R., et al., 2015. Neonicotinoid pesticides severely affect honey bee queens.Scientific Reports,  6: p. 14621.
  75. Pettis, J.S., et al., 2012. Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften,  99: p. 153-158.
  76. Lu, C., K.M. Warchol, and R.A. Callahan, 2014. Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder. Bulletin of Insectology,  67(1): p. 125-130.
  77. Cutler, G.C. and C.D. Scott-Dupree, 2007. Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. Journal of Economic Entomology,  100(3): p. 765-772.
  78. Cutler, G.C., C.D. Scott-Dupree, and D.M. Drexler, 2014. Honey bees, neonicotinoids and bee incident reports: the Canadian situation. Pest Management Science,  70: p. 779-83.
  79. Scholer, J. and V. Krischik, 2014. Chronic exposure of imidacloprid and clothianidin reduce queen survival, foraging, and nectar storing in colonies of Bombus impatiens. PLoS One,  9: p. e91573.
  80. Gill, R.J. and N.E. Raine, 2014. Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Functional Ecology,  28: p. 1459-1471.
  81. Feltham, H., K. Park, and D. Goulson, 2014. Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology,  23(3): p. 317-323.
  82. Mommaerts, V., et al., 2010. Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology,  19(1): p. 207-215.
  83. Gels, J.A., D.W. Held, and D.A. Potter, 2002. Hazards of insecticides to the bumble bees Bombus impatiens (Hymenoptera : Apidae) foraging on flowering white clover in turf. Journal of Economic Entomology,  95(4): p. 722-728.
  84. Whitehorn, P.R., et al., 2012. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science,  336(6079): p. 351-352.
  85. Larson, J.L., C.T. Redmond, and D.A. Potter, 2013. Assessing insecticide hazard to bumble bees foraging on flowering weeds in treated lawns. PLoS One,  8: p. e66375.
  86. Gill, R.J., O. Ramos-Rodriguez, and N.E. Raine, 2012. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature,  491: p. 105-108.
  87. Schmuck, R., T. Stadler, and H.W. Schmidt, 2003. Field relevance of a synergistic effect observed in the laboratory between an EBI fungicide and a chloronicotinyl insecticide in the honeybee (Apis mellifera L, Hymenoptera). Pest Management Science,  59(3): p. 279-286.