Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by nosema ceranae

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Vidau, Cyril ^a,b   Diogon, Marie ^a,b   Aufauvre, Julie ^a,b   Fontbonne, Régis ^a,b   Viguès, Bernard ^a,b   Brunet, Jean Luc ^c   Texier, Catherine ^b   Biron, David G ^a,b   Blot, Nicolas ^a,b   Alaoui, Hicham ^a,b   Belzunces, Luc P ^c   Delbac, Frédéric ^a,b  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITÉ BLAISE PASCAL   (France)

^c Laboratoire de Toxicologie Environnementale   (France)

Author keywords

[No Author keywords available]

Indexed keywords

7 ETHOXYCOUMARIN DEETHYLASE; FIPRONIL; GLUTATHIONE TRANSFERASE; INSECTICIDE; THIACLOPRID; UNCLASSIFIED DRUG; PYRAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; THIAZINE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; BEE DISEASE; CONTROLLED STUDY; DETOXIFICATION; ENZYME ACTIVITY; EXPERIMENTAL INFECTION; FAT BODY; HONEYBEE; LD 50; MICROSPORIDIA; MIDGUT; MORTALITY; NONHUMAN; NOSEMA; NOSEMOSIS; SPOROGENESIS; ANIMAL; BEE; DRUG EFFECT; MICROBIOLOGY; PATHOGENICITY;

APIS MELLIFERA; HEXAPODA; NOSEMA CERANAE;

ANIMALS; BEES; INSECTICIDES; NOSEMA; PYRAZOLES; PYRIDINES; THIAZINES;

EID: 79959640170     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021550     Document Type: Article

References (57)

1. Gallai N, Salles J-M, Settele J, Vaissière BE, (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68: 810-821.
2. Ratnieks FL, Carreck NL, (2010) Ecology. Clarity on honey bee collapse? Science 327: 152-153.
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.
4. Maxim L, van der Sluijs JP, (2007) Uncertainty: Cause or effect of stakeholders' debates?: Analysis of a case study: The risk for honeybees of the insecticide Gaucho®. Science of The Total Environment 376: 1-17.
5. OEPP/EPPO (2003) Environmental risk assessment scheme for plant protection products. Bull OEPP/EPPO 33: 141-145.
6. Halm MP, Rortais A, Arnold G, Tasei JN, Rault S, (2006) New risk assessment approach for systemic insecticides: the case of honey bees and imidacloprid (Gaucho). Environ Sci Technol 40: 2448-2454.
7. Rortais A, Arnold G, Halm M-P, 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.
8. Suchail S, Guez D, Belzunces LP, (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem 20: 2482-2486.
9. Desneux N, Decourtye A, Delpuech JM, (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52: 81-106.
10. 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.
11. Hardstone MC, Scott JG, (2010) Is Apis mellifera more sensitive to insecticides than other insects? Pest Manag Sci 66: 1171-1180.
12. Yu SJ, Robinson FA, Nation JL, (1984) Detoxication capacity in the honey bee, Apis mellifera L. Pesticide Biochemistry and Physiology 22: 360-368.
13. Terriere LC, (1984) Induction of Detoxication Enzymes in Insects. Annual Review of Entomology 29: 71-88.
14. 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.
15. Holmstrup M, Bindesbol AM, Oostingh GJ, Duschl A, Scheil V, et al. (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408: 3746-3762.
16. Cameron PJ, Walker GP, Hodson AJ, Kale AJ, Herman TJB, (2009) Trends in IPM and insecticide use in processing tomatoes in New Zealand. Crop Protection 28: 421-427.
17. Ericsson JD, Kabaluk JT, Goettel MS, Myers JH, (2007) Spinosad interacts synergistically with the insect pathogen Metarhizium anisopliae against the exotic wireworms Agriotes lineatus and Agriotes obscurus (Coleoptera: Elateridae). J Econ Entomol 100: 31-38.
18. Mohamed AK, Pratt JP, Nelson FR, (1987) Compatibility of Metarhizium anisopliae var. anisopliae with chemical pesticides. Mycopathologia 99: 99-105.
19. Ladas A, (1972) Der einfluss verschiedener konstitutions- und umweltfaktoren auf die anfã"lligkeit der honigbiene (Apis mellifica l.) gegenãœber zwei insektiziden pflanzenschutzmitteln. Apidologie 3: 55-78.
20. Alaux C, Brunet JL, Dussaubat C, Mondet F, Tchamitchan S, et al. (2009) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol 12: 774-782.
21. Higes M, Martin-Hernandez R, Meana A, (2010) Nosema ceranae in Europe: an emergent type C nosemosis*. Apidologie 41: 375-392.
22. Mayack C, Naug D, (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol 100: 185-188.
23. Mayack C, Naug D, (2010) Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. J Insect Physiol 56: 1572-1575.
24. Antunez K, Martin-Hernandez R, Prieto L, Meana A, Zunino P, et al. (2009) Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ Microbiol 11: 2284-2290.
25. Dussaubat C, Maisonnasse A, Alaux C, Tchamitchan S, Brunet JL, et al. (2010) Nosema spp. infection alters pheromone production in honey bees (Apis mellifera). J Chem Ecol 36: 522-525.
26. Higes M, Martin R, Meana A, (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92: 93-95.
27. Kievits JB, E, (2009) Neurotoxiques systémiques, un risque pour les abeilles? Pesticides news pp. 76.
28. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
29. de Sousa G, Cuany A, Brun A, Amichot M, Rahmani R, et al. (1995) A microfluorometric method for measuring ethoxycoumarin-O-deethylase activity on individual Drosophila melanogaster abdomens: interest for screening resistance in insect populations. Anal Biochem 229: 86-91.
30. Habig WH, Pabst MJ, Jakoby WB, (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249: 7130-7139.
31. Paxton RJ, Klee J, Korpela S, Fries I, (2007) Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38: 558-565.
32. Higes M, Martin-Hernandez R, Botias C, Bailon EG, Gonzalez-Porto AV, et al. (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10: 2659-2669.
33. Bride JM, Cuany A, Amichot M, Brun A, Babault M, et al. (1997) Cytochrome P-450 field insecticide tolerance and development of laboratory resistance in grape vine populations of Drosophila melanogaster (Diptera: Drosophilidae). J Econ Entomol 90: 1514-1520.
34. Enayati AA, Ranson H, Hemingway J, (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14: 3-8.
35. 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. Environ Toxicol Chem 28: 113-122.
36. Farenhorst M, Mouatcho JC, Kikankie CK, Brooke BD, Hunt RH, et al. (2009) Fungal infection counters insecticide resistance in African malaria mosquitoes. Proc Natl Acad Sci U S A 106: 17443-17447.
37. Mariyono J, (2008) Direct and indirect impacts of integrated pest management on pesticide use: a case of rice agriculture in Java, Indonesia. Pest Manag Sci 64: 1069-1073.
38. Weddle PW, Welter SC, Thomson D, (2009) History of IPM in California pears-50 years of pesticide use and the transition to biologically intensive IPM. Pest Manag Sci 65: 1287-1292.
39. Purwar JP, Sachan GC, (2006) Synergistic effect of entomogenous fungi on some insecticides against Bihar hairy caterpillar Spilarctia obliqua (Lepidoptera: Arctiidae). Microbiol Res 161: 38-42.
40. Pachamuthu P, Kamble ST, (2000) In vivo study on combined toxicity of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) strain ESC-1 with sublethal doses of chlorpyrifos, propetamphos, and cyfluthrin against German cockroach (Dictyoptera: Blattellidae). J Econ Entomol 93: 60-70.
41. 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.
42. Al Mazraawi MS, (2007) Interaction effects between Beauveria bassiana and imidacloprid against Thrips tabaci (Thysanoptera: Thripidae). Commun Agric Appl Biol Sci 72: 549-555.
43. Farenhorst M, Knols BG, Thomas MB, Howard AF, Takken W, et al. (2010) Synergy in efficacy of fungal entomopathogens and permethrin against West African insecticide-resistant Anopheles gambiae mosquitoes. PLoS One 5: e12081.
44. Furlong MJ, Groden E, (2001) Evaluation of synergistic interactions between the Colorado potato beetle (Coleoptera: Chrysomelidae) pathogen Beauveria bassiana and the insecticides, imidacloprid, and cyromazine. J Econ Entomol 94: 344-356.
45. Serebrov VV, Gerber ON, Maliarchuk AA, Martem'ianov VV, Alekseev AA, et al. (2006) [The effect of entomopathogenic fungi on the activity of detoxicating enzymes of larvae of bee pyralid Galleria mellonella L. (Lepidoptera, Pyralidee) and the role of detoxicating enzymes in the formation of the insect' resistance to entomopathogenic fungi]. Izv Akad Nauk Ser Biol pp. 712-718.
46. Felix RC, Muller P, Ribeiro V, Ranson H, Silveira H, (2010) Plasmodium infection alters Anopheles gambiae detoxification gene expression. BMC Genomics 11: 312.
47. Gui Z, Hou C, Liu T, Qin G, Li M, et al. (2009) Effects of insect viruses and pesticides on glutathione S-transferase activity and gene expression in Bombyx mori. J Econ Entomol 102: 1591-1598.
48. Shiotsuki T, Kato Y, (1999) Induction of carboxylesterase isozymes in Bombyx mori by E. coli infection. Insect Biochem Mol Biol 29: 731-736.
49. Tchankouo-Nguetcheu S, Khun H, Pincet L, Roux P, Bahut M, et al. (2010) Differential protein modulation in midguts of Aedes aegypti infected with chikungunya and dengue 2 viruses. PLoS One 5.
50. Zibaee A, Bandani AR, Tork M, (2009) Effect of the entomopathogenic fungus, Beauveria bassiana, and its secondary metabolite on detoxifying enzyme activities and acetylcholinesterase (AChE) of the Sunn pest, Eurygaster integriceps (Heteroptera: Scutellaridae). Biocontrol Science and Technology 19: 485-498.
51. Alaux C, Folschweiller M, McDonnell C, Beslay D, Cousin M, et al. (2011) Pathological effects of the microsporidium Nosema ceranae on honey bee queen physiology (Apis mellifera). Journal of Invertebrate Pathology 106: 380-385.
52. Le Goff G, Hilliou F, Siegfried BD, Boundy S, Wajnberg E, et al. (2006) Xenobiotic response in Drosophila melanogaster: sex dependence of P450 and GST gene induction. Insect Biochem Mol Biol 36: 674-682.
53. Alizadeh A, Samih MA, Izadi H, (2007) Compatibility of Verticillium lecani (Zimm.) with several pesticides. Commun Agric Appl Biol Sci 72: 1011-1015.
54. Li DP, Holdom DG, (1994) Effects of Pesticides on Growth and Sporulation of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes). Journal of Invertebrate Pathology 63: 209-211.
55. da Silva Cruz A, da Silva-Zacarin EC, Bueno OC, Malaspina O, (2010) Morphological alterations induced by boric acid and fipronil in the midgut of worker honeybee (Apis mellifera L.) larvae: Morphological alterations in the midgut of A. mellifera. Cell Biol Toxicol 26: 165-176.
56. Vidau C, Brunet JL, Badiou A, Belzunces LP, (2009) Phenylpyrazole insecticides induce cytotoxicity by altering mechanisms involved in cellular energy supply in the human epithelial cell model Caco-2. Toxicol In Vitro 23: 589-597.
57. Lassiter TL, MacKillop EA, Ryde IT, Seidler FJ, Slotkin TA, (2009) Is fipronil safer than chlorpyrifos? Comparative developmental neurotoxicity modeled in PC12 cells. Brain Res Bull 78: 313-322.