Neonicotinoid-coated Zea mays seeds indirectly affect honeybee performance and pathogen susceptibility in field trials

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Alburaki, Mohamed ^a,b,e   Boutin, Sébastien ^a   Mercier, Pierre Luc ^a,b   Loublier, Yves ^d   Chagnon, Madeleine ^c   Derome, Nicolas ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b Direction de l'Innovation Scientifique Ettechnologique   (Canada)

^c UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^d France and University of Paris Sud   (France)

^e UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; NEONICOTINOID; PESTICIDE RESIDUE; PESTICIDE;

ACETYLCHOLINESTERASE GENE; ADULT; ANIMAL EXPERIMENT; ARTICLE; BROOD QUEEN CELL VIRUS; CANADA; CONTROLLED STUDY; DEFORMED WING VIRUS; FLOWER; FORAGING BEHAVIOR; HONEY; HONEYBEE; LIQUID CHROMATOGRAPHY; MAIZE; MASS SPECTROMETRY; NONHUMAN; POLLEN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VARROOSIS; VIRUS; VIRUS LOAD; ANIMAL; BEE; CHEMISTRY; DISEASE PREDISPOSITION; DRUG EFFECTS; GENE; GENETICS; METABOLISM; ORGANIC FARMING; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGICAL STRESS; PLANT SEED; TOXICITY; VARROIDAE; VIROLOGY;

ACUTE BEE PARALYSIS VIRUS; APIS MELLIFERA; APOIDEA; DEFORMED WING VIRUS; ZEA MAYS;

ACETYLCHOLINESTERASE; ANIMALS; BEES; DISEASE SUSCEPTIBILITY; FLOWERS; GENES, INSECT; ORGANIC AGRICULTURE; PESTICIDE RESIDUES; PESTICIDES; POLLEN; SEEDS; STRESS, PHYSIOLOGICAL; VARROIDAE; ZEA MAYS;

EID: 84930679156     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125790     Document Type: Article

References (74)

1. Johnson RM, Ellis MD, Mullin CA, Frazier M. Pesticides and honey bee toxicity - USA. Apidologie. 2010; 41(3):312-31. doi: 10.1051/Apido/2010018 PMID: WOS:000279029200008.
2. Bacandritsos N, Granato A, Budge G, Papanastasiou I, Roinioti E, Caldon M, et al. Sudden deaths and colony population decline in Greek honey bee colonies. J Invertebr Pathol. 2010; 105(3):335-40. doi: 10.1016/j.jip.2010.08.004 PMID: 20804765.
3. Martin SJ, Ball BV, Carreck NL. Prevalence and persistence of deformed wing virus (DWV) in untreated or acaricide-treated Varroa destructor infested honey bee (Apis mellifera) colonies. J Apicult Res. 2010; 49(1):72-9. doi: 10.3896/Ibra.1.49.1.10 PMID: WOS:000276090500010.
4. Zioni N, Soroker V, Chejanovsky N. Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1-deformed wing virus recombinant (VDV-1-DWV) in the head of the honey bee. Virology. 2011; 417(1):106-12. doi: 10.1016/J.Virol.2011.05.009 PMID: WOS:000293820300013.
5. Bromenshenk JJ, Henderson CB, Wick CH, Stanford MF, Zulich AW, Jabbour RE, et al. Iridovirus and microsporidian linked to honey bee colony decline. PloS one. 2010; 5(10):e13181. doi: 10.1371/journal.pone.0013181 PMID: 20949138; PubMed Central PMCID: PMC2950847.
6. Fries I. Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology. 2010; 103:S73-S9. doi: 10.1016/J.Jip.2009.06.017 PMID: WOS:000273993100009.
7. Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P. Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Appl Environ Microbiol. 2012; 78(4):981-7. doi: 10.1128/AEM.06537-11 PMID: 22179240; PubMed Central PMCID: PMC3273028.
8. Van der Sluijs JP, Simon-Delso N, Goulson D, Maxim L, Bonmatin J-M, Belzunces LP. Neonicotinoids, bee disorders and the sustainability of pollinator services. Current Opinion in Environmental Sustainability. 2013; 5(0):293-305. doi: 10.1016/j.cosust.2013.05.007
9. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, Vanengelsdorp D, et al. High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PloS one. 2010; 5(3):e9754. doi: 10.1371/journal.pone.0009754 PMID: 20333298; PubMed Central PMCID: PMC2841636.
10. Vanbergen AJ, The Insect Pollinators Initiative. Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ. 2013; 11:251-9.
11. Wu JY, Smart MD, Anelli CM, Sheppard WS. Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. J Invertebr Pathol. 2012; 109(3):326-9. doi: 10.1016/j.jip.2012.01.005 PMID: 22285445.
12. Aizen MA, Garibaldi LA, Cunningham SA, Klein AM. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Annals of Botany. 2009; 103(9):1579-88. doi: 10.1093/aob/mcp076 PMID: 19339297
13. Withgott J. Pollination migrates to top of conservation agenda. Bioscience. 1999; 49:857-62. PMID: 10337200
14. Kremen C, Ricketts T. Global perspectives on pollination disruptions. Conservation Biology. 2000; 14:1226-8.
15. Morse RA, Calderone NW. "The value of honey bees as pollinators of U.S. crops in 2000". Cornell University, Ithaca, New York. 2000.
16. NAS. Status of pollinators in North America. National Academy Press, Washington, DC. 2007.
17. Atkins EL. Injury to honey bees by poisoning. The hive and the honey bee, Dadant and Sons ed. Hamilton, IL1992 1992. 1324 p.
18. Van der Zee R, Pisa L, Andonov S, Brodschneider R, Charriere JD, Chlebo R, et al. Managed honey bee colony losses in Canada, China, Europe, Israel and Turkey, for the winters of 2008-9 and 2009-10. J Apicult Res. 2012; 51(1):91-114. doi: 10.3896/Ibra.1.51.1.12 PMID: WOS:000299995700012.
19. Guzman-Novoa E, Eccles L, Calvete Y, Mcgowan J, Kelly PG, Correa-Benitez A. Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie. 2010; 41(4):443-50. doi: 10.1051/Apido/2009076 PMID: WOS:000280290600004.
20. Charvet R, Katouzian-Safadi M, Colin ME, Marchand PA, Bonmatin JM. [Systemic insecticides: new risk for pollinator insects]. Annales pharmaceutiques francaises. 2004; 62(1):29-35. PMID: 14747770.
21. Flaherty DL, Gilley JB, Prieto HR, Romani J, Soares J. Pesticide Honeybee Kill Survey during Citrus Bloom in Tulare County. Am Bee J. 1977; 117(4):220-&. PMID: WOS:A1977DB02400006.
22. Bourke JB, Morse RA. Documenting Honey Bee Pesticide Loss. Am Bee J. 1982; 122(11):780-. PMID: WOS:A1982PN57500012.
23. Smirle MJ, Winston ML. Intercolony Variation in Pesticide Detoxification by the Honey-Bee (Hymenoptera, Apidae). Journal of economic entomology. 1987; 80(1):5-8. PMID: WOS:A1987G884800004.
24. Davis AR. The Study of Insecticide Poisoning of Honeybee Brood. Bee World. 1989; 70(4):163-74. PMID: WOS:A1989CK19000003.
25. Haynes KF. Sublethal Effects of Neurotoxic Insecticides on Insect Behavior. Annu Rev Entomol. 1988; 33:149-68. doi: 10.1146/Annurev.En.33.010188.001053 PMID: WOS:A1988L532100008.
26. Desneux N, Decourtye A, Delpuech JM. The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol. 2007; 52:81-106. doi: 10.1146/annurev.ento.52.110405.091440 PMID: 16842032.
27. Gill RJ, Ramos-Rodriguez O, Raine NE. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature. 2012; 491(7422):105-8. doi: 10.1038/nature11585 PMID: 23086150; PubMed Central PMCID: PMC3495159.
28. Schneider CW, Tautz J, Grunewald B, Fuchs S. RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PloS one. 2012; 7(1):e30023. doi: 10.1371/journal.pone.0030023 PMID: 22253863; PubMed Central PMCID: PMC3256199.
29. Leonardi MG, Cappellozza S, Ianne P, Cappellozza L, Parenti P, Giordana B. Effects of the topical application of an insect growth regulator (fenoxycarb) on some physiological parameters in the fifth instar larvae of the silkworm Bombyx mori. Comp Biochem Phys B. 1996; 113(2):361-5. doi: 10.1016/0305-0491(95)02051-9 PMID: WOS:A1996UD42800019.
30. Mackenzie KE, Winston ML. Effects of Sublethal Exposure to Diazinon on Longevity and Temporal Division of Labor in the Honey Bee (Hymenoptera, Apidae). Journal of economic entomology. 1989; 82 (1):75-82. PMID: WOS:A1989T153800013.
31. Cox RL, Wilson WT. Effects of Permethrin on the Behavior of Individually Tagged Honey Bees, Apis- Mellifera L (Hymenoptera, Apidae). Environmental entomology. 1984; 13(2):375-8. PMID: WOS: A1984ST28600009.
32. Vandame R, Meled M, Colin ME, Belzunces LP. Alteration of the Homing-Flight in the Honey-Bee Apis- Mellifera L Exposed to Sublethal Dose of Deltamethrin. Environ Toxicol Chem. 1995; 14(5):855-60.: doi: 10.1897/1552-8618(1995)14[855:Aothit]2.0.Co;2 PMID: WOS:A1995QV45600017.
33. Decourtye A, Devillers J, Genecque E, Menach KL, Budzinski H, Cluzeau S, et al. Comparative Sublethal Toxicity of Nine Pesticides on Olfactory Learning Performances of the Honeybee Apis mellifera. Archives of environmental contamination and toxicology. 2005; 48(2):242-50. doi: 10.1007/s00244-003-0262-7 PMID: 15750780
34. Gauthier M. State of the Art on Insect Nicotinic Acetylcholine Receptor Function in Learning and Memory. In: Thany S, editor. Insect Nicotinic Acetylcholine Receptors. Advances in Experimental Medicine and Biology. 683: Springer New York; 2010. p. 97-115. PMID: 20737792
35. Williamson SM, Wright GA. Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol. 2013; 216(10):1799-807. doi: 10.1242/Jeb.083931 PMID: WOS:000318483600013.
36. Henry M, Béguin M, Requier F, Rollin O, Odoux J-F, Aupinel P, et al. A Common Pesticide Decreases Foraging Success and Survival in Honey Bees. Science. 2012; 336(6079):348-50. doi: 10.1126/science.1215039 PMID: 22461498
37. Decourtye A, Devillers J, Aupinel P, Brun F, Bagnis C, Fourrier J, et al. Honeybee tracking with microchips: a new methodology to measure the effects of pesticides. Ecotoxicology. 2011; 20(2):429-37. doi: 10.1007/S10646-011-0594-4 PMID: WOS:000287245000013.
38. Tanner G, Czerwenka C. LC-MS/MS Analysis of Neonicotinoid Insecticides in Honey: Methodology and Residue Findings in Austrian Honeys. Journal of agricultural and food chemistry. 2011; 59 (23):12271-7. doi: 10.1021/Jf202775m PMID: WOS:000297608400001.
39. Boily M, Sarrasin B, Deblois C, Aras P, Chagnon M. Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids, atrazine and glyphosate: laboratory and field experiments. Environmental science and pollution research international. 2013; 20(8):5603-14. doi: 10.1007/s11356-013-1568-2 PMID: 23443944.
40. Beekman M, Ratnieks FLW. Long-range foraging by the honey-bee, Apis mellifera L. Funct Ecol. 2000; 14(4):490-6. doi: 10.1046/J.1365-2435.2000.00443.X PMID: WOS:000089054800011.
41. Garnery L, Cornuet JM, Solignac M. Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Molecular ecology. 1992; 1(3):145-54. PMID: 1364272.
42. Garnery L, Solignac M, Celebrano G, Cornuet JM. A Simple Test Using Restricted Pcr-Amplified Mitochondrial-DNA to Study the Genetic-Structure of Apis-Mellifera L. Experientia. 1993; 49(11):1016-21. doi: 10.1007/Bf02125651 PMID: WOS:A1993MH40600013.
43. Alburaki M, Moulin S, Legout H, Alburaki A, Garnery L. Mitochondrial structure of Eastern honeybee populations from Syria, Lebanon and Iraq. Apidologie. 2011; 42(5):628-41. doi: 10.1007/S13592-011-0062-4 PMID: WOS:000293971900009.
44. Arias MC, Sheppard WS. Molecular phylogenetics of honey bee subspecies (Apis mellifera L.) inferred from mitochondrial DNA sequence. Molecular phylogenetics and evolution. 1996; 5(3):557-66. Epub 1996/06/01. PMID: 8744768.
45. Walsh PS, Metzger DA, Higuchi R. Chelex-100 as a Medium for Simple Extraction of DNA for Pcr-Based Typing from Forensic Material. Biotechniques. 1991; 10(4):506-13. PMID: WOS: A1991FG60000021.
46. Chomczynski P. A Reagent for the Single-Step Simultaneous Isolation of Rna, DNA and Proteins from Cell and Tissue Samples. Biotechniques. 1993; 15(3):532-&. PMID: WOS:A1993LW41700037.
47. Tentcheva D, Gauthier L, Bagny L, Fievet J, Dainat B, Cousserans F, et al. Comparative analysis of deformed wing virus (DWV) RNA in Apis mellifera L. and Varroa destructor. Apidologie. 2006; 37:41-50. doi: 10.1051/apido:2005057
48. Furgala B, Lee P. Acute bee paralysis virus, a cytoplasmic insect virus. Virology. 1966; 29:346-8. doi: 10.1016/0042-6822(66)90042-0 PMID: 5943541
49. Scharlaken B, de Graaf DC, Goossens K, Brunain M, Peelman LJ, Jacobs FJ. Reference gene selection for insect expression studies using quantitative real-time PCR: The head of the honeybee, Apis mellifera, after a bacterial challenge. J Insect Sci. 2008; 8. PMID: WOS:000255795400001.
50. Loublier Y, Morlot M, Ricard M, Richard C, Estermann O, Leclair P, et al. Eléments de caractérisation du miel de Sophora du Japon (Sophora japonica L.). Pollen. 2003; 13:363-72.
51. Louveaux J, Albisetti M, Delangue M, Theurkauff M. Les modalités de l'adaptation des abeilles (Apis mellifera L.) au milieu naturel. Annales de l'abeille. 1966; 9:323-50.
52. Louveaux J. The acclimatization of bees to a heather region Bee world. 1973; 54:105-11.
53. Williams GR, Dietemann V, Ellis JD, Neumann P. An update on the COLOSS network and the "BEE-BOOK: standard methodologies for Apis mellifera research". J Apicult Res. 2012; 51(2):151-3. doi: 10.3896/Ibra.1.51.2.01 PMID: WOS:000302295500001.
54. Pinheiro JC, Bates DM. Mixed-Effects Models in S and S-PLUS: Springer; 2000.
55. Bates D, Maechler M, Bolker B, Walker S. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7. http://CRAN.R-project.org/package=lme4.2014. doi: 10.1016/j.jsps.2012.11.002 PMID: 24653595
56. Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest: Tests in Linear Mixed Effects Models. R package version 2.0-20. http://CRANR-projectorg/package=lmerTest. 2014. doi: 10.1186/1471-2164-15-862 PMID: 25283306
57. Shapiro SS, Wilk MB. An analysis of variance test for normality (complete samples). Biometrika. 1965; 52(3-4):591-611. doi: 10.1093/biomet/52.3-4.591 PMID: 5858975
58. Welch BL. The generalisation of student's problems when several different population variances are involved. Biometrika. 1947; 34(1-2):28-35. PMID: 20287819.
59. Team RDC. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2011. doi: 10.1016/j.neuroimage.2011.01.013 PMID: 21238596
60. EFSA (European Food Safety Authority). Statement on the findings in recent studies investigating sublethal effects in bees of some neonicotinoids in consideration of the uses currently authorised in Europe. EFSA J. 2012; 10:2752. doi: 10.2903/j.efsa.2012.2752
61. Van Dijk TC, Van Staalduinen MA, Van der Sluijs JP. Macro-invertebrate decline in surface water polluted with imidacloprid. PloS one. 2013; 8(5):e62374. doi: 10.1371/journal.pone.0062374 PMID: 23650513; PubMed Central PMCID: PMC3641074.
62. Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PloS one. 2012; 7(1):e29268. doi: 10.1371/journal.pone.0029268 PMID: 22235278; PubMed Central PMCID: PMC3250423.
63. Stewart SD, Lorenz GM, Catchot AL, Gore J, Cook D, Skinner J, et al. Potential exposure of pollinators to neonicotinoid insecticides from the use of insecticide seed treatments in the mid-southern United States. Environmental science & technology. 2014; 48(16):9762-9. doi: 10.1021/es501657w PMID: 25010122.
64. Chen YP, Pettis JS, Collins A, Feldlaufer MF. Prevalence and transmission of honeybee viruses. Appl Environ Microbiol. 2006; 72(1):606-11. doi: 10.1128/AEM.72.1.606-611.2006 PMID: 16391097; PubMed Central PMCID: PMC1352288.
65. Rosenkranz P, Aumeier P, Ziegelmann B. Biology and control of Varroa destructor. J Invertebr Pathol. 2010; 103 Suppl 1:S96-119. doi: 10.1016/j.jip.2009.07.016 PMID: 19909970.
66. Shen M, Yang X, Cox-Foster D, Cui L. The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology. 2005; 342(1):141-9. doi: 10.1016/j.virol.2005.07.012 PMID: 16109435.
67. Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G, Varricchio P, et al. Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS pathogens. 2012; 8(6):e1002735. doi: 10.1371/journal.ppat.1002735 PMID: 22719246; PubMed Central PMCID: PMC3375299.
68. Bowen-Walker P, Martin S, Gunn A. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite varroa jacobsoni Oud. J Invertebr Pathol. 1999; 73:101-6. doi: 10.1006/jipa.1998.4807 PMID: 9878295
69. Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, Nazzi F, et al. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc Natl Acad Sci U S A. 2013; 110(46):18466-71. doi: 10.1073/pnas.1314923110 PMID: 24145453; PubMed Central PMCID: PMC3831983.
70. Alaux C, Brunet JL, Dussaubat C, Mondet F, Tchamitchan S, Cousin M, et al. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environmental microbiology. 2010; 12(3):774-82. doi: 10.1111/j.1462-2920.2009.02123.x PMID: 20050872; PubMed Central PMCID: PMC2847190.
71. Vidau C, Diogon M, Aufauvre J, Fontbonne R, Vigues B, Brunet JL, et al. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PloS one. 2011; 6(6):e21550. doi: 10.1371/journal.pone.0021550 PMID: 21738706; PubMed Central PMCID: PMC3125288.
72. Aufauvre J, Biron DG, Vidau C, Fontbonne R, Roudel M, Diogon M, et al. Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee. Scientific reports. 2012; 2:326. doi: 10.1038/srep00326 PMID: 22442753; PubMed Central PMCID: PMC3310228.
73. Cutler GC, Scott-Dupree CD. Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. Journal of economic entomology. 2007; 100(3):765-72. PMID: 17598537.
74. Wang R, Wang Z, Yang H, Wang Y, Deng A. Highly sensitive and specific detection of neonicotinoid insecticide imidacloprid in environmental and food samples by a polyclonal antibody-based enzyme-linked immunosorbent assay. J Sci Food Agric. 2012; 92(6):1253-60. doi: 10.1002/jsfa.4691 PMID: 22083888.