Pesticide residues and bees - A risk assessment

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Sanchez Bayo, Francisco ^a   Goka, Koichi ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b INSTITUTE FOR ENVIRONMENTAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPYRIFOS; CYHALOTHRIN; ERGOSTEROL; FUNGICIDE; IMIDACLOPRID; INSECTICIDE; NEONICOTINOID; PESTICIDE; PYRETHROID; THIAMETHOXAM; UNCLASSIFIED DRUG; PESTICIDE RESIDUE;

ARTICLE; BUMBLEBEE; CHEMICAL INTERACTION; CHEMICAL PHENOMENA; CONTAMINATED ORGANISM; ENVIRONMENTAL EXPOSURE; HONEYBEE; INTOXICATION; NONHUMAN; POLLEN; PREVALENCE; RESIDUE ANALYSIS; RISK ASSESSMENT; TOXICITY TESTING; ANIMAL; BEE; DIET; DRUG EFFECTS; HONEY; LARVA; LD50; PHYSIOLOGY; RISK FACTOR; TIME;

ANIMALS; BEES; DIET; ENVIRONMENTAL EXPOSURE; HONEY; LARVA; LETHAL DOSE 50; PESTICIDE RESIDUES; POLLEN; RISK ASSESSMENT; RISK FACTORS; TIME FACTORS;

EID: 84899582629     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094482     Document Type: Article

References (99)

1. Osborne JL (2012) Ecology: Bumblebees and pesticides. Nature 491: 43-45.
2. Marletto F, Patetta A, Manino A (2003) Laboratory assessment of pesticide toxicity to bumble bees. Bulletin of Insectology 56: 155-158.
3. Mommaerts V, Smagghe G (2011) Side-effects of pesticides on the pollinator Bombus: An overview. In: Stoytcheva M, editor. Pesticides in the Modern World - Pests Control and Pesticides Exposure and Toxicity Assessment. Rijeka, Croatia: InTech. pp. 508-552.
4. Klein A-M, Vaissile BE, Cane JH, Steffan-Dewenter I, Cunningham SA, et al. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274: 303-313. (Pubitemid 47055453)
5. Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, et al. (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conservation Biology 12: 8-17. (Pubitemid 28153802)
6. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, et al. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25: 345-353.
7. Heard TA (1999) The role of stingless bees in crop pollination. Annual Review of Entomology 44: 183-206.
8. Graystock P, Yates K, Evison SEF, Darvill B, Goulson D, et al. (2013) The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. Journal of Applied Ecology 50: 1207-1215.
9. Goka K, Okabe K, Yoneda M (2006) Worldwide migration of parasitic mites as a result of bumblebee comercialization. Population Ecology 48: 285-291.
10. Kenta T, Inari N, Nagamitsu T, Goka K, Hiura T (2007) Commercialized European bumblebee can cause pollination disturbance: an experiment on seven native plant species in Japan. Biological Conservation 134: 298-309. (Pubitemid 44826960)
11. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, et al. (2007) A metagenomic survey of microbes in honey bee Colony Collapse Disorder. Science 318: 283-287. (Pubitemid 47574857)
12. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, et al. (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Science USA 108: 662-667.
13. Thompson H, Ball R, Brown M, Bew M (2003) Varroa destructor resistance to pyrethroid treatments in the United Kingdom. Bulletin of Insectology 56: 175-181.
14. Underwood RM, vanEngelsdorp D (2007) Colony Collapse Disorder: have we seen this before? Bee Culture 135: 13-15.
15. Buczek K (2009) Honey bee colony collapse disorder (CCD) [Zespo masowego giniecia pszczoy miodnej (CCD)]. Annales Universitatis Mariae Curie-Skodowska Sectio DD, Medicina Veterinaria 64: 1-6.
16. Maini S, Medrzycki P, Porrini C (2010) The puzzle of honey bee losses: a brief review. Bulletin of Insectology 63: 153-160.
17. Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity - USA. Apidologie 41: 312-331.
18. Pettis J, vanEngelsdorp D, Johnson J, Dively G (2012) Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99: 153-158.
19. Vidau C, Diogon M, Aufauvre J, Fontbonne R, Vigues B, et al. (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PloS One: e21550.
20. Goulson D (2013) An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology 50: 977-987.
21. Blacquière T, Smagghe G, van Gestel C, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21: 973-992.
22. Mommaerts V, Reynders S, Boulet J, Besard L, Sterk G, et al. (2010) Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19: 207-215.
23. Aliouane Y, El-Hassani AK, Gary V, Armengaud C, Lambin M, et al. (2009) Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior. Environmental Toxicology and Chemistry 28: 113-122.
24. Williams GR, Tarpy DR, vanEngelsdorp D, Chauzat M-P, Cox-Foster DL, et al. (2010) Colony Collapse Disorder in context. BioEssays 32: 845-846.
25. Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annual Review of Entomology 53: 191-208. (Pubitemid 351341938)
26. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, et al. (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PloS One 5: e9754.
27. Rennich K, Pettis J, vanEngelsdorp D, Bozarth R, Eversole H, et al. (2012) 2011-2012 National Honey Bee Pests and Diseases Survey Report. USDA. 17 p.
28. Stoner KA, Eitzer BD (2013) Using a hazard quotient to evaluate pesticide residues detected in pollen trapped from honey bees (Apis mellifera) in Connecticut. PLoS One 8: e77550.
29. Chauzat MP, Carpentier P, Martel AC, Bougeard S, Cougoule N, et al. (2009) Influence of pesticide residues on honey bee (Hymenoptera: Apidae) colony health in France. Environmental Entomology 38: 514-523.
30. Chauzat M-P, Faucon J-P, Martel A-C, Lachaize J, Cougoule N, et al. (2006) A survey of pesticide residues in pollen loads collected by honey bees in France. Journal of Economic Entomology 99: 253-262. (Pubitemid 44638103)
31. Bernal J, Garrido-Bailon E, Nozal MJd, Gonzalez-Porto AV, Martin-Hernandez R, et al. (2010) Overview of pesticide residues in stored pollen and their potential effect on bee colony (Apis mellifera) losses in Spain. Journal of Economic Entomology 103: 1964-1971.
32. Choudhary A, Sharma DC (2008) Dynamics of pesticide residues in nectar and pollen of mustard (Brassica juncea (L.) Czern.) grown in Himachal Pradesh (India). Environmental Monitoring and Assessment 144: 143-150.
33. Thompson HM (2001) Assessing the exposure and toxicity of pesticides to bumblebees (Bombus sp.). Apidologie 32: 305-321.
34. Greig-Smith PW, Thompson HM, Hardy AR, Bew MH, Findlay E, et al. (1994) Incidents of poisoning of honeybees (Apis mellifera) by agricultural pesticides in Great Britain 1981-1991. Crop Protection 13: 567-581.
35. Villa S, Vighi M, Finizio A, Bolchi Serini G (2000) Risk assessment for honeybees from pesticide-exposed pollen. Ecotoxicology 9: 287-297.
36. VanEngelsdorp D, Speybroeck N, Evans JD, Nguyen BK, Mullin C, et al. (2010) Weighing risk factors associated with Bee Colony Collapse Disorder by classification and regression tree analysis. Journal of Economic Entomology 103: 1517-1523.
37. Tennekes HA, Sánchez-Bayo F (2012) Time-dependent toxicity of neonicotinoids and other toxicants: implications for a new approach to risk assessment. Journal of Environmental & Analytical Toxicology S4: S4-001.
38. Halm M-P, Rortais A, Arnold G, Taséi JN, Rault S (2006) New risk assessment approach for systemic insecticides: the case of honey bees and imidacloprid (Gaucho). Environmental Science & Technology 40: 2448-2454.
39. EPA (2012) White Paper in Support of the Proposed Risk Assessment Process for Bees. In: Office of Chemical Safety and Pollution Prevention OoPP, Environmental Fate and Effects Division, editor. Washington, D. C. pp. 275.
40. Zhu W, Schmehl DR, Mullin CA, Frazier JL (2014) Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLoS One 9: e77547.
41. Geoghegan TS, Kimberly JH, Scheringer M (2013) Predicting honeybee exposure to pesticides from vapour drift using a combined pesticide emission and atmospheric transport model. SETAC Australasia - Multidisciplinary approaches to managing environmental pollution. Melbourne 1-3 October. pp. 174.
42. Henry Ml, Beguin M, Requier F, Rollin O, Odoux JFo, et al. (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336: 348-350.
43. Whitehorn PR, O'Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336: 351-352.
44. Scott-Dupree CD, Conroy L, Harris CR (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: 177-182.
45. Helson BV, Barber KN, Kingsbury PD (1994) Laboratory toxicology of six forestry insecticides to four species of bee (Hymenoptera: Apoidea). Archives of Environmental Contamination and Toxicology 27: 107-114. (Pubitemid 24175500)
46. Tasei JN (2002) Impact of agrochemicals on non-Apis bees. In: Devillers J, Pham-Delegue MH, editors. Honey bees: estimating the environmental impact of chemicals. pp. 101-131.
47. Chauzat M-P, Martel A-C, Cougoule N, Porta P, Lachaize J, et al. (2011) An assessment of honeybee colony matrices, Apis mellifera (Hymenoptera: Apidae) to monitor pesticide presence in continental France. Environmental Toxicology and Chemistry 30: 103-111.
48. Pohorecka K, Skubida P, Miszczak A, Semkiw P, Sikorski P, 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: 115-134.
49. Balayiannis G, Balayiannis P (2008) Bee honey as an environmental bioindicator of pesticides' occurrence in six agricultural areas of Greece. Archives of Environmental Contamination and Toxicology 55: 462-470.
50. Blasco C, Fernandez M, Pena A, Lino C, Silveira MI, et al. (2003) Assessment of pesticide residues in honey samples from Portugal and Spain. Journal of Agricultural and Food Chemistry 51: 8132-8138.
51. Rissato SR, Galhiane MS, de Almeida MV, Gerenutti M, Apon BM (2007) Multiresidue determination of pesticides in honey samples by gas chromatography-mass spectrometry and application in environmental contamination. Food Chemistry 101: 1719-1726. (Pubitemid 44466215)
52. Amit C, Sharma DC (2008) Pesticide residues in honey samples from Himachal Pradesh (India). Bulletin of Environmental Contamination and Toxicology 80: 417-422.
53. Schmuck R, Schöning R, Stork A, Schramel O (2001) Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Management Science 57: 225-238. (Pubitemid 32179089)
54. Stoner KA, Eitzer BD (2012) Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS One 7: e39114.
55. Dively GP, 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.
56. Byrne FJ, Visscher PK, Leimkuehler B, Fischer D, Grafton-Cardwell EE, et al. (2014) Determination of exposure levels of honey bees foraging on flowers of mature citrus trees previously treated with imidacloprid. Pest Management Science 70: 470-482.
57. Serra-Bonvehí J, Orantes-Bermejo J (2010) Acaricides and their residues in Spanish commercial beeswax. Pest Management Science 66: 1230-1235.
58. Wu JY, Anelli CM, Sheppard WS (2011) Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS One 6: e14720.
59. Landis WG, Chapman PM (2011) Well past time to stop using NOELs and LOELs. Integrated Environmental Assessment and Management 7: vi-viii.
60. Fox DR, Billoir E, Charles S, Delignette-Muller ML, Lopes C (2012) What to do with NOECS/NOELS-prohibition or innovation? Integrated Environmental Assessment and Management 8: 764-766.
61. Tomlin CDS (2009) The e-Pesticide Manual. In: Tomlin CDS, editor. 12 ed. Surrey, U.K.: British Crop Protection Council.
62. Suchail S, Guez D, Belzunces LP (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environmental Toxicology and Chemistry 20: 2482-2486. (Pubitemid 34117869)
63. Dechaume-Moncharmont F-X, Decourtye A, Hennequet-Hantier C, Pons O, Pham-Delegue M-H (2003) Statistical analysis of honeybee survival after chronic exposure to insecticides. Environmental Toxicology and Chemistry 22: 3088-3094. (Pubitemid 37485243)
64. Thompson HM, Hunt LV (1999) Extrapolating from honeybees to bumblebees in pesticide risk assessment. Ecotoxicology 8: 147-166. (Pubitemid 29471936)
65. Wijngaarden RPAV, Brock TCM, van den Brink PJ (2005) Threshold levels for effects of insecticides in freshwater ecosystems: a review. Ecotoxicology 14: 355-380. (Pubitemid 40576939)
66. Mattila HR, Harris JL, Otis GW (2001) Timing of production of winter bees in honey bee (Apis mellifera) colonies. Insectes Sociaux 48: 88-93.
67. Iwasa T, Motoyama N, Ambrose JT, Roe RM (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection 23: 371-378. (Pubitemid 38355801)
68. Pilling ED, Jepson PC (1993) Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera) . Pesticide Science 39: 293-297.
69. Biddinger DJ, Robertson JL, Mullin C, Frazier J, Ashcraft SA, et al. (2013) Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS One 8: e72587.
70. Suchail S, Debrauwer L, Belzunces LP (2004) Metabolism of imidacloprid in Apis mellifera. Pest Management Science 60: 291-296. (Pubitemid 38268800)
71. Sánchez-Bayo F (2009) From simple toxicological models to prediction of toxic effects in time. Ecotoxicology 18: 343-354.
72. Tennekes HA, Sánchez-Bayo F (2013) The molecular basis of simple relationships between exposure concentration and toxic effects with time. Toxicology 309: 39-51.
73. Oliveira RA, Roat TC, Carvalho SM, Malaspina O (2013) Side-effects of thiamethoxam on the brain and midgut of the africanized honeybee Apis mellifera (Hymenopptera: Apidae). Environmental Toxicology 28: (in press) DOI:10.1002/tox.21842.
74. Chauzat M-P, Faucon J-P (2007) Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in France. Pest Management Science 63: 1100-1106. (Pubitemid 350033356)
75. Schmuck R, Stadler T, Schmidt HW (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: 279-286. (Pubitemid 36288083)
76. Rortais A, Arnold G, Halm MP, Touffet-Briens F (2005) Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36: 71-83. (Pubitemid 40560983)
77. Jacob CRO, Soares HM, Carvalho SM, Nocelli RCF, Malaspina O (2013) Acute toxicity of fipronil to the stingless bee Scaptotrigona postica Latreille. Bulletin of Environmental Contamination and Toxicology 90: 69-72.
78. Girolami V, Marzaro M, Vivan L, Mazzon L, Greatti M, et al. (2012) Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implication. Journal of Applied Entomology 136: 17-26.
79. Kovac H, Stabentheiner A, Schmaranzer S (2010) Thermoregulation of water foraging honeybees - Balancing of endothermic activity with radiative heat gain and functional requirements. Journal of Insect Physiology 56: 1834-1845.
80. Thompson HM (2010) Risk assessment for honey bees and pesticides-recent developments and 'new issues'. Pest Management Science 66: 1157-1162.
81. Tapparo A, Marton D, Giorio C, Zanella A, Solda L, et al. (2012) Assessment of the environmental exposure of honeybees to particulate matter containing neonicotinoid insecticides coming from corn coated seeds. Environmental Science & Technology 46: 2592-2599.
82. Mineau P, Harding KM, Whiteside M, Fletcher MR, Garthwaite D, et al. (2008) Using reports of bee mortality in the field to calibrate laboratory-derived pesticide risk indices. Environmental Entomology 37: 546-554. (Pubitemid 351685366)
83. Tasei JN, Ripault G, Rivault E (2001) Hazards of imidacloprid seed coating to Bombus terrestris (Hymenoptera: Apidae) when applied to sunflower. Journal of Economic Entomology 94: 623-627. (Pubitemid 33750039)
84. Hsieh Y-N, Liu L-F, Wang Y-S (1998) Uptake, translocation and metabolism of the herbicide molinate in tobacco and rice. Pesticide Science 53: 149-154. (Pubitemid 28286548)
85. Vieira RF, Sumner DR (1999) Application of fungicides to foliage through overhead sprinkler irrigation - a review. Pesticide Science 55: 412-422. (Pubitemid 29186051)
86. Higes M, Martín-Hernández R, Martínez-Salvador A, Garrido-Bailón E, González-Porto AV, et al. (2010) A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environmental Microbiology Reports 2: 243-250.
87. Schmuck R (2001) Ecotoxicological profile of the insecticide thiacloprid. Pflanzenschutz-Nachrichten Bayer 54: 161-184.
88. Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491: 105-108.
89. Suchail S, Sousa Gd, Rahmani R, Belzunces LP (2004) In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L. Pest Management Science 60: 1056-1062.
90. Decourtye A, Armengaud C, Renou M, Devillers J, Cluzeau S, et al. (2004) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pesticide Biochemistry and Physiology 78: 83-92. (Pubitemid 38836702)
91. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52: 81-106. (Pubitemid 46133563)
92. Teeters BS, Johnson RM, Ellis MD, Siegfried BD (2012) Using video-tracking to assess sublethal effects of pesticides on honey bees (Apis mellifera L.). Environmental Toxicology and Chemistry 31: 1349-1354.
93. Moffett JO, Macdonald RH, Levin MD (1970) Toxicity of carbaryl-contaminated pollen to adult honey bees. Journal of Economic Entomology 63: 475-476.
94. Johansen CA, Rincker CM, George DA, Mayer DF, Kious CW (1984) Effects of aldicarb and its biologically active metabolites on bees. Environmental Entomology 13: 1386-1398.
95. van der Sluijs JP, Simon-Delso N, Goulson D, Maxim L, Bonmatin J-M, et al. (2013) Neonicotinoids, bee disorders and the sustainability of pollinator services. Current Opinion in Environmental Sustainability 5: 293-305.
96. Laurino D, Manino A, Patetta A, Porporato M (2013) Toxicity of neonicotinoid insecticides on different honey bee genotypes. Bulletin of Insectology 66: 119-126.
97. Cresswell J (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20: 149-157.
98. Pilling E, Campbell P, Coulson M, Ruddle N, Tornier I (2014) 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.
99. Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, 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 110: 18466-18471.