Acaricide, Fungicide and Drug Interactions in Honey Bees (Apis mellifera)

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Johnson, Reed M ^a,b   Dahlgren, Lizette ^a   Siegfried, Blair D ^a   Ellis, Marion D ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACARICIDE; AMITRAZ; COUMAFOS; CYTOCHROME P450; FENPYROXIMATE; FLUVALINATE; FUNGICIDE; PROCHLORAZ; THYMOL; UNCLASSIFIED DRUG;

APIS MELLIFERA; ARTICLE; CHEMICAL INTERACTION; CHEMICAL PEST CONTROL; CONTROLLED STUDY; DETOXIFICATION; ENZYME INDUCTION; ENZYME INHIBITION; LD 50; NONHUMAN; PROTEIN FUNCTION;

ACARICIDES; ANIMALS; ANTI-INFECTIVE AGENTS; BEEKEEPING; BEES; CYTOCHROME P-450 ENZYME SYSTEM; DRUG INTERACTIONS; FUNGICIDES, INDUSTRIAL; HONEY; METABOLIC DETOXICATION, DRUG; NITRILES; PESTICIDES; PYRETHRINS; TOLUIDINES; VARROIDAE;

EID: 84873859691     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054092     Document Type: Article

References (76)

1. Bogdanov S, (2006) Contaminants of bee products. Apidologie 37: 1-18 doi:10.1051/apido:2005043.
2. Chauzat MP, Faucon JP, (2007) Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in France. Pest Manag Sci 63: 1100-1106 doi:10.1002/ps.1451.
3. 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 doi:10.1371/journal.pone.0009754.
4. Rosenkranz P, Aumeier P, Ziegelmann B, (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103: S96-S119 doi:10.1016/j.jip.2009.07.016.
5. Le Conte Y, Ellis MD, Ritter W, (2010) Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 41: 353-363 doi:10.1051/apido/2010017.
6. Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C, et al. (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41: 332-352 doi:10.1051/apido/2010014.
7. Boecking O, Genersch E, (2008) Varroosis- the ongoing crisis in bee keeping. J Verbrauch Lebensm 3: 221-228 doi:10.1007/s00003-008-0331-y.
8. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, et al. (2009) Colony collapse disorder: a descriptive study. PLoS ONE 4: e6481 doi:10.1371/journal.pone.0006481.
9. Lodesani M, Colombo M, Spreafico M, (1995) Ineffectiveness of Apistan® treatment against the mite Varroa jacobsoni Oud in several districts of Lombardy (Italy). Apidologie 26: 67-72 doi:10.1051/apido:19950109.
10. Elzen PJ, Westervelt D, (2002) Detection of coumaphos resistance in Varroa destructor in Florida. Am Bee J 142: 291-292.
11. Bogdanov S, (2004) Beeswax: quality issues today. Bee World 85: 46-50.
12. Bogdanov S, Imdorf A, Kilchenmann V, (1998) Residues in wax and honey after Apilife VAR® treatment. Apidologie 29: 513-524 doi:10.1051/apido:19980604.
13. Martel AC, Zeggane S, Aurières C, Drajnudel P, Faucon JP, et al. (2007) Acaricide residues in honey and wax after treatment of honey bee colonies with Apivar® or Asuntol® 50. Apidologie 38: 534-544 doi:10.1051/apido:2007038.
14. Rademacher E, Harz M, (2006) Oxalic acid for the control of varroosis in honey bee colonies - a review. Apidologie 37: 98-120 doi:10.1051/apido:2005063.
15. Adamczyk S, Lázaro R, Pérez-Arquillué C, Conchello P, Herrera A, (2005) Evaluation of residues of essential oil components in honey after different anti-Varroa treatments. J Agric Food Chem 53: 10085-10090 doi:10.1021/jf051813f.
16. Mussen EC, (2008) Fungicides toxic to bees? From the UC Apiaries 17: 1-3.
17. Atkins EL (1992) Injury to honey bee by poisoning. In: Graham JE, editor. The Hive and the Honey Bee. Hamilton, IL: Dadant and Sons. 1153-1208.
18. Mussen EC, Lopez JE, Peng CYS, (2004) Effects of selected fungicides on growth and development of larval honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environ Entomol 33: 1151-1154 doi:10.1603/0046-225X-33.5.1151.
19. vanEngelsdorp D, Evans JD, Donovall L, Mullin C, Frazier M, et al. (2009) "Entombed pollen": a new condition in honey bee colonies associated with increased risk of colony mortality. J Invertebr Pathol 101: 147-149 doi:10.1016/j.jip.2009.03.008.
20. Pilling ED, Bromley-Challenor KAC, Walker CH, Jepson PC, (1995) Mechanism of synergism between the pyrethroid insecticide λ-Cyhalothrin and the imidazole fungicide prochloraz, in the honeybee (Apis mellifera L.). Pestic Biochem Physiol 51: 1-11 doi:10.1006/pest.1995.1001.
21. Vandame R, Belzunces LP, (1998) Joint actions of deltamethrin and azole fungicides on honey bee thermoregulation. Neurosci Lett 251: 57-60 doi:10.1016/S0304-3940(98)00494-7.
22. Johnson RM, Pollock HS, Berenbaum MR, (2009) Synergistic interactions between in-hive miticides in Apis mellifera. J Econ Entomol 102: 474-479 doi:10.1603/029.102.0202.
23. Thompson H, Wilkins S, (2003) Assessment of the synergy and repellency of pyrethroid/fungicide mixtures. Bull Insectology 56: 131-134.
24. Colin ME, Belzunces LC, (1992) Evidence of synergy between prochloraz and deltamethrin in Apis mellifera L: a convenient biological approach. Pestic Sci 36: 115-119 doi:10.1002/ps.2780360206.
25. Bliss CI, (1939) The toxicity of poisons applied jointly. Ann Appl Biol 26: 585-615 doi:10.1111/j.1744-7348.1939.tb06990.x.
26. Robertson JL, Savin NE, Preisler HK, Russell RM (2007) Bioassays with arthropods. Boca Raton: CRC Press. 224 p.
27. Garcia D, Bujons J, Vale C, Suñol C, (2006) Allosteric positive interaction of thymol with the GABAA receptor in primary cultures of mouse cortical neurons. Neuropharmacology 50: 25-35 doi:10.1016/j.neuropharm.2005.07.009.
28. Johnson RM, Ellis MD, Mullin CA, Frazier M, (2010) Pesticides and honey bee toxicity - USA. Apidologie 41: 312-331 doi:10.1051/apido/2010018.
29. Yu SJ (2008) The toxicology and biochemistry of insecticides. Baton Roca: CRC Press. 296 p.
30. Sanders W, Sanders C, (1979) Toxicity of antibacterial agents: mechanism of action on mammalian cells. Annu Rev Pharmacol Toxicol 19: 53-83 doi:10.1146/annurev.pa.19.040179.000413.
31. Zhang Y, Yeh J, Mara A, Ju R, Hines J, et al. (2006) A chemical and genetic approach to the mode of action of fumagillin. Chem Biol 13: 1001-1009 doi:10.1016/j.chembiol.2006.07.010.
32. Fungicide Resistance Action Committee (2012) FRAC Code List 2012. Available: http://www.frac.info/frac/publication/anhang/FRAC-Code-List2011-final.pdf Accessed: 24 August 2012.
33. Insecticide Resistance Action Committee (2012) In:Sparks T, Salgado V, editors. MoA Classification Feb 2012. Available: http://www.irac-online.org/content/uploads/MoA-classification.pdf Accessed: 11 December 2012.
34. Tenson T, Lovmar M, Ehrenberg M, (2003) The mechanism of action of macrolides, lincosamides and streptogramin B reveals the nascent peptide exit path in the ribosome. J Mol Biol 330: 1005-1014 doi:10.1016/S0022-2836(03)00662-4.
35. Johnson RM, Wen Z, Schuler MA, Berenbaum MR, (2006) Mediation of pyrethroid insecticide toxicity to honey bees (Hymenoptera: Apidae) by cytochrome P450 monooxygenases. J Econ Entomol 99: 1046-1050 doi:10.1603/0022-0493-99.4.1046.
36. R Development Core Team (2012) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
37. Finney DJ (1971) Probit analysis. Cambridge: Cambridge University Press. 350 p.
38. Savin NE, Robertson JL, Russell RM, (1977) A critical evaluation of bioassay in insecticide research: likelihood ratio tests of dose-mortality regression. Bull ESA 23: 257-266.
39. Mao W, Schuler M, Berenbaum M (2011) CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proc Natl Acad Sci U S A doi:10.1073/pnas.1109535108.
40. De-Oliveira AC, Fidalgo-Neto AA, Paumgartten FJ, (1999) In vitro inhibition of liver monooxygenases by beta-ionone, 1,8-cineole, (-)-menthol and terpineol. Toxicology 135: 33-41 doi:10.1016/S0300-483X(99)00043-8.
41. Usmani AK, Abd-Elghafar SF, Knowles CO, (1995) Amitraz effect on the pharmacokinetics of permethrin in Helicoverpa zea (Lepidoptera: Noctuidae). J Econ Entomol 88: 1580-1585.
42. Liu MY, Plapp FW Jr, (1992) Mechanism of formamidine synergism of pyrethroids. Pestic Biochem Physiol 43: 134-140 doi:10.1016/0048-3575(92)90027-W.
43. Orr GL, Orr N, Cornfield L, Gole JWD, Downer RGH, (1990) Interaction of formamidine pesticides with insect neural octopamine receptors: effects on radioligand binding and cyclic AMP production. Pestic Sci 30: 285-294 doi:10.1002/ps.2780300305.
44. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, et al. (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol 15: 615-636 doi:10.1111/j.1365-2583.2006.00672.x.
45. Corta E, Bakkali A, Berrueta LA, Gallo B, Vicente F, (1999) Kinetics and mechanism of amitraz hydrolysis in aqueous media by HPLC and GC-MS. Talanta 48: 189-199 doi:10.1016/S0039-9140(98)00237-9.
46. Corta E, Bakkali A, Barranco A, Berrueta LA, Gallo B, et al. (2000) Study of the degradation products of bromopropylate, chlordimeform, coumaphos, cymiazole, flumethrin and tau-fluvalinate in aqueous media. Talanta 52: 169-180 doi:10.1016/S0039-9140(00)00333-7.
47. Cao LC, Honeyman TW, Cooney R, Kennington L, Scheid CR, et al. (2004) Mitochondrial dysfunction is a primary event in renal cell oxalate toxicity. Kidney Int 66: 1890-1900 doi:10.1111/j.1523-1755.2004.00963.x.
48. Meimaridou E, Jacobson J, Seddon AM, Noronha-Dutra AA, Robertson WG, et al. (2005) Crystal and microparticle effects on MDCK cell superoxide production: oxalate-specific mitochondrial membrane potential changes. Free Radic Biol Med 38: 1553-1564 doi:10.1016/j.freeradbiomed.2005.02.020.
49. Tremolada P, Bernardinelli I, Colombo M, Spreafico M, Vighi M, (2004) Coumaphos distribution in the hive ecosystem: case study for modeling applications. Ecotoxicology 13: 589-601 doi:10.1023/B:ECTX.0000037193.28684.05.
50. Bogdanov S, Kilchenmann V, Imdorf A, (1998) Acaricide residues in some bee products. J Apic Res 37: 57-67.
51. Haarmann T, Spivak M, Weaver D, Weaver B, Glenn T, (2002) Effects of fluvalinate and coumaphos on queen honey bees (Hymenoptera: Apidae) in two commercial queen rearing operations. J Econ Entomol 95: 28-35 doi:10.1603/0022-0493-95.1.28.
52. Sokol R, (1996) The influence of a multimonth persistence of Fluwarol in a hive of a honey bee colony. Medycyna Weterynaryjna 52: 718-720.
53. Wallner K, (1999) Varroacides and their residues in bee products. Apidologie 30: 235-238 doi:10.1051/apido:19990212.
54. Medici SK, Castro A, Sarlo EG, Marioli JM, Eguaras MJ, (2012) The concentration effect of selected acaricides present in beeswax foundation on the survival of Apis mellifera colonies. J Apic Res 51: 164-168 doi:10.3896/IBRA.1.51.2.03.
55. 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 doi:10.1371/journal.pone.0014720.
56. Wu JY, Smart MD, Anelli CM, Sheppard WS, (2012) Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. J Invert Path 109: 326-329 doi:10.1016/j.jip.2012.01.005.
57. Kubik M, Nowacki J, Pidek A, Warakomska Z, Michalczuk L, et al. (2000) Residues of captan (contact) and difenoconazole (systemic) fungicides in bee products from an apple orchard. Apidologie 31: 531-541 doi:10.1051/apido:2000144.
58. Willoughby L, Batterham P, Daborn P, (2007) Piperonyl butoxide induces the expression of cytochrome P450 and glutathione S-transferase genes in Drosophila melanogaster. Pest Manag Sci 63: 803-808 doi:10.1002/ps.1391.
59. Sergent T, Dupont I, Jassogne C, Ribonnet L, van der Heiden E, et al. (2009) CYP1A1 induction and CYP3A4 inhibition by the fungicide imazalil in the human intestinal Caco-2 cells-comparison with other conazole pesticides Toxicol Lett. 184: 159-168 doi:10.1016/j.toxlet.2008.11.009.
60. Mao W, Rupasinghe SG, Johnson RM, Zangerl AR, Schuler MA, et al. (2009) Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comp Biochem Physiol B Biochem Mol Biol 154: 427-434 doi:10.1016/j.cbpb.2009.08.008.
61. Johnson RM, Mao W, Pollock HS, Niu G, Schuler M, et al. (2012) Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PLoS ONE 7: e31051 doi:10.1371/journal.pone.0031051.
62. Chaves A, Shea D, Danehower D, (2008) Analysis of chlorothalonil and degradation products in soil and water by GC/MS and LC/MS. Chemosphere 71: 629-638 doi:10.1016/j.chemosphere.2007.11.015.
63. Suzuki T, Nojiri H, Isono H, Ochi T, (2004) Oxidative damages in isolated rat hepatocytes treated with the organochlorine fungicides captan, dichlofluanid and chlorothalonil. Toxicology 204: 97-107 doi:10.1016/j.tox.2004.06.025.
64. Kuhn PJ, (1984) Mode of action of carboximides. British Mycological Society Symposium 9: 155-183.
65. Anke T, (1995) The antifungal strobilurins and their possible ecological role. Can J Bot 73: 940-945.
66. Motoba K, Suzuki T, Uchida M, (1992) Effect of a new acaricide, fenpyroximate, on energy metabolism and mitochondrial morphology in adult female Tetranychus urticae (two-spotted spider mite). Pestic Biochem Physiol 43: 37-44 doi:10.1016/0048-3575(92)90017-T.
67. Sherer TB, Richardson JR, Testa CM, Seo BB, Panov AV, et al. (2007) Mechanism of toxicity of pesticides acting at complex I: relevance to environmental etiologies of Parkinson's disease. J Neurochem 100: 1469-1479 doi:10.1111/j.1471-4159.2006.04333.x.
68. Kale M, Rathore N, John S, Bhatnagar D, (1999) Lipid peroxidative damage on pyrethroid exposure and alterations in antioxidant status in rat erythrocytes: a possible involvement of reactive oxygen species. Toxicol Lett 105: 197-205 doi:10.1016/S0378-4274(98)00399-3.
69. Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Cambridge: Harvard University Press. 318 p.
70. Hawthorne D, Dively G, (2011) Killing them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger honey bees. PLoS ONE 6: e26796 doi:10.1371/journal.pone.0026796.
71. Gregorc GA, Bowen ID, (2000) Histochemical characterization of cell death in honeybee larvae midgut after treatment with Paenibacillus larvae, amitraz, and oxytetracycline. Cell Biol Int 24: 319-324 doi:10.1006/cbir.1999.0490.
72. Miyachi Y, Yoshioka A, Imamura S, Niwa Y, (1986) Effect of antibiotics on the generation of reactive oxygen species. J Invest Dermatol 86: 449-453 doi:10.1111/1523-1747.ep12285793.
73. Elzen PJ, Elzen GW, Rubink W, (2003) Comparative susceptibility of European and Africanized honey bee (Hymenoptera: Apidae) ecotypes to several insecticide classes. Southwestern Entomologist 28: 255-260.
74. Dai PL, Wang Q, Sun JH, Liu F, Wang X, et al. (2010) Effects of sublethal concentrations of bifenthrin and deltamethrin on fecundity, growth, and development of the honeybee Apis mellifera ligustica. Environ Toxicol Chem 29: 644-649 doi:10.1002/etc.67.
75. Gill RJ, Ramos-Rodriguez O, Raine NE, (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491: 105-108 doi:10.1038/nature11585.
76. Aliano NP, Ellis MD, Siegfried BD, (2006) Acute contact toxicity of oxalic acid to Varroa destructor (Acari: Varroidae) and their Apis mellifera (Hymenoptera: Apidae) hosts in laboratory bioassays. J Econ Entomol 99: 1579-1582 doi:10.1603/0022-0493-99.5.1579.