Effects of realistic doses of atrazine, metolachlor, and glyphosate on lipid peroxidation and diet-derived antioxidants in caged honey bees (Apis mellifera)

Environmental Science and Pollution Research

Volumn 22, Issue 11, 2015, Pages 8010-8021

  Helmer, Stephanie Hedrei ^a   Kerbaol, Anahi ^a   Aras, Philippe ^a   Jumarie, Catherine ^a   Boily, Monique ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

All trans retinol; Apis mellifera; Carotenoids; TBARS; Tocopherol

Indexed keywords

APIS MELLIFERA; ZEA MAYS;

ACETAMIDE DERIVATIVE; ALPHA TOCOPHEROL; ANTIOXIDANT; ATRAZINE; CAROTENOID; GLYCINE; GLYPHOSATE; HERBICIDE; METOLACHLOR; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANALOGS AND DERIVATIVES; ANIMAL; BEE; DRUG EFFECTS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID PEROXIDATION; METABOLISM; NONPARAMETRIC TEST; OXIDATIVE STRESS;

ACETAMIDES; ALPHA-TOCOPHEROL; ANIMALS; ANTIOXIDANTS; ATRAZINE; BEES; CAROTENOIDS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GLYCINE; HERBICIDES; LIPID PEROXIDATION; OXIDATIVE STRESS; STATISTICS, NONPARAMETRIC; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84929843681     PISSN: 09441344     EISSN: 16147499     Source Type: Journal    
DOI: 10.1007/s11356-014-2879-7     Document Type: Article

References (63)

1. Álvarez R, Vaz B, Gronemeyer H, de Lera AR (2013) Functions, therapeutic applications, and synthesis of retinoids and carotenoids. Chem Rev. doi:10.1021/cr400126u
2. ARLA (Agence de réglementation de la lutte antiparasitaire) (2007) Décision de réévaluation: atrazine (Évaluation environnementale). Santé Canada, Sécurité des produits de consommation, RVD2007-05
3. Arshavsky VY (2009) Vision: the retinoid cycle in Drosophila. Curr Biol R96–8. doi:10.1016/j.cub.2009.12.039
4. Bahadorani S, Bahadorani P, Phillips JP, Hilliker AJ (2008) The effects of vitamin supplementation on Drosophila life span under normoxia and under oxidative stress. J Gerontol A Biol Sci Med Sci 63:35–42
5. Berry JA, Hood WM, Pietravalle S, Delaplane KS (2013) Field-level sublethal effects of approved bee hive chemicals on honey bees (Apis mellifera L). PLoS ONE 8(10):e76536. doi:10.1371/journal.pone.0076536
6. Boily M, Thibodeau J, Bisson M (2009) Retinoid metabolism (LRAT, REH) in the liver and plasma retinoids of bullfrog, Rana catesbeiana, in relation to agricultural contamination. Aquat Toxicol 91:118–125
7. Boily M, Sarrasin B, DeBlois C, Aras P, Chagnon M (2013) Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids, atrazine and glyphosate: laboratory and field experiments. Environ Sci Pollut Res 20:5603–5614
8. Bonnefont D, Legrand A, Peynet J, Emerit J, Delattre J, Galli A (1989) Distribution of thiobarbituric acid-reactive substances in lipoproteins and proteins in serum. Clin Chem 35:2054–2058
9. Boucher C (2013) Rapport sur les mortalités de colonies d’abeilles observées à la suite de l’hivernage de 2012-2013. L’abeille 35:8–10
10. Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
11. Casani R (2000) Vitamin E. Kirk-Othmer encyclopedia of chemical technology. doi:10.1002/0471238961.2209200103011901.a01
12. Chantarudee A, Phuwapraisirisan P, Kimura K, Okuyama M, Mori H, Kimura A, Chanchao C (2012) Chemical constituents and free radical scavenging activity of corn pollen collected from Apis mellifera hives compared to floral corn pollen of Nan, Thailand. BMC Complement Alter Med 12:45
13. Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A et al (2013) Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS ONE 8(8):e72016. doi:10.1371/journal.pone.0072016
14. Dobšíková R, Blahová J, Modrá H, Škorič M, Svobodová Z (2011) The effect of acute exposure to herbicide Gardoprim Plus Gold 500 SC on haematological and biochemical indicators and histopathological changes in common carp (Cyprinus carpio L.). Acta Vet BRNO 80:359–363
15. Farjan M, Dmitryjuk M, Lipiński Z, Biernat-Łopieńska E, Żółtowska K (2012) Supplementation of the honey bee diet with vitamin C: the effect on the antioxidative system of Apis mellifera carnica brood at different stages. J Api Res 51:263–270
16. García-Plazaola JI, Becerril JM (1999) A rapid high-performance liquid chromatography method to measure lipophilic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochem Anal 10:307–313
17. George DGM, Gatehouse AMR (2013) Oxidative stress enzymes in Busseola fusca. Int J Curr Microbiol App Sci 2:485–495
18. Giovannucci DR, Stephenson RS (1999) Identification and distribution of dietary precursors of the Drosophila visual pigment chromophore: analysis of carotenoids in wild type and ninaD mutants by HPLC. Vis Res 39:219–229
19. Gorse I, Rivard L (2011) Bilan des ventes de pesticides au Québec pour l’année 2008, Québec, Ministère du Développement durable, de l’Environnement et des Parcs, ISBN (PDF) 978-2-550-61586-6, 85 p
20. Grotto D, Santa Maria L, Valentini C, Paniz C, Schmitt G et al (2009) Importance of the lipid peroxidation biomarkers and methodological aspects for malondialdehyde quantification. Quim Nova 32:169–174
21. Hahn DA, Denlinger DL (2007) Meeting the energetic demands of insect diapause: nutrient storage and utilization. J Insect Physiol 53:760–773
22. Halme A, Cheng M, Hariharan IK (2010) Retinoids regulate a developmental checkpoint for tissue regeneration in Drosophila. Curr Biol 20:458–463
23. Hanganu D, Olah N, Vlase L, Marculedscu A, Pintea A (2012) Chemical research of carotenoids from Chenopodium bonus henricus L. (Chenopodiaceae). Farm 60:840–849
24. Horváth G, Molnar P, Farkas A, Szabo LG, Turcsi E, Deli J (2010) Separation and identification of carotenoids in flowers of Chelidonium majus L. and inflorescences of Solidago canadensis L. Chromatographia 71:S103–S108
25. Hsu CY, Hsieh YS (2013) Oxidative stress decreases in the trophocytes and fat cells of worker honeybees during aging. Biogerontology. doi:10.1007/s10522-013-9485-9
26. ISQ (Institut de la statistique du Québec), MAPAQ (Ministère de l’Agriculture, des Pêcheries et de l'Alimentation du Québec) (2013) Profil sectoriel de l’industrie bioalimentaire du Québec, édition 2013. Gouvernement du Québec, ISBN 978-2-550-70028-9 (PDF)
27. Jasper R, Locatelli GO, Pilati C, Locatelli C (2012) Evaluation of biochemical, hematological and oxidative parameters in mice exposed to the herbicide glyphosate-Roundup®. Interdiscip Toxicol 5:133–140
28. Johnson RM, Dahlgren L, Siegfried BD, Ellis MD (2013) Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLoS ONE 8(1):e54092. doi:10.1371/journal.pone.0054092
29. Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity. Apidologie 41:312–332
30. Kane MA, Folias AE, Napoli JL (2008) HPLC/UV quantification of retinal, retinol, and retinyl esters in serum and tissues. Anal Biochem 378:71–79
31. Kayser H (1982) Carotenoids in insects. In: Britton G, Goodwin TW (eds) Carotenoid chemistry and biochemistry. Pergamon Press, Toronto, pp 195–210
32. Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One 7:e29268. doi:10.1371/journal.pone.0029268
33. Lenkowski JR, McLaughlin KA (2010) Acute atrazine exposure disrupts matrix metalloproteinases and retinoid signaling during organ morphogenesis in Xenopus laevis. J Appl Toxicol 30:582–589
34. Mann RM, Hyne RV, Choung CB, Wilson SP (2009) Amphibians and agricultural chemicals: review of the risks in a complex environment. Environ Pollut 157:2903–2927
35. Maini S, Medrzycki P, Porrini C (2010) The puzzle of honey bee losses: a brief review. Bull Insectol 63:153–160
36. Mueller L, Boehm V (2011) Antioxidant activity of β-carotene compounds in different in vitro assays. Molecules 16:1055–1069. doi:10.3390/molecules16021055
37. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, Vanengelsdorp D, Pettis JS (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5(3):e9754. doi:10.1371/journal.pone.0009754
38. Murvoll KM, Skaare JU, Jensen H, Jenssen BM (2007) Associations between persistent organic pollutants and vitamin status in Brünnich’s guillemot and common eider hatchlings. Sci Total Environ 381:134–145
39. Nakamuraa A, Stiebler R, Fantappi MR, Fialho E, Masudaa H, Oliveira MF (2007) Effects of retinoids and juvenoids on moult and on phenoloxidase activity in the blood-sucking insect Rhodnius prolixus. Acta Trop 103:222–230
40. Ndayibagira A, Spear PA (1999) Esterification and hydrolysis of vitamin A in liver of brook trout (Salvelinus fontinalis) and the influence of a coplanar polychlorinated biphenyl. Comp Biochem Physiol C 122:317–325
41. Nwani CD, Lakra WS, Nagpure NS, Kumar R, Kushwaha B, Srivastava SK (2010) Toxicity of the herbicide atrazine: effects on lipid peroxidation and activities of antioxidant enzymes in the freshwater fish Channa Punctatus (Bloch). Int J Environ Res Public Health 7:3298–3312
42. Ohkawa H, Ohishi N, Tagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Chem 95:351–358
43. Otis GW, Wheeler DE, Buck N, Mattila HR (2004) Storage proteins in winter honey bees. Apiacata 38:352–357
44. Paganelli A, Gnazzo V, Acosta H, López SL, Carrasco AE (2010) Glyphosate-based herbicides produce teratogenic effects on vertebrates by impairing retinoic acid signaling. Chem Res Toxicol 23:1586–1595
45. Potts SG, Roberts SPM, Dean R, Marris G, Brown MA, Jones R, Neumann P, Settele J (2010) Declines of managed honey bees and beekeepers in Europe. J Api Res 49:15–22
46. Rael LT, Thomas GW, Craun ML, Curtis CG, Bar-Or R, Bar-Or D (2004) Lipid peroxidation and the thiobarbituric acid assay: standardization of the assay when using saturated and unsaturated fatty acids. J Biochem Mol Biol 37:749–752
47. Rehman S, Rehman S, Waliullah MIS (2012) Chlorpyrifos-induced neuro-oxidative damage in bee. Toxicol Environ Health Sci 4:30–36. doi:10.1007/s13530-012-0114-9
48. Rousse P, Gourdon F, Roubaud M, Chiroleu F, Quilici S (2009) Biotic and abiotic factors affecting the flight activity of Fopius arisanus, an egg-pupal parasitoid of fruit fly pests. Environ Entomol 38:896–903
49. Shete V, Quadro L (2013) Mammalian metabolism of β-Carotene: gaps in knowledge. Nutrients 5:4849–4868. doi:10.3390/nu5124849
50. 2+ homeostasis in rat erythrocytes with atrazine treatment: positive modulation by vitamin E. Mol Cell Biochem 340:231–238
51. Široká Z, Drastichová J (2004) Biochemical markers of aquatic environment contamination-cytochrome P450 in fish. A review. Acta Vet Brno 73:123–132
52. Sleeman JM, Brown J, Steffen D, Jones D, Roberston J, Holladay S (2008) Relationships among aural abscesses, organochlorine compounds, and vitamin A in free-ranging eastern Box turtles (Terrapene Carolina carolina). J Wild Dis 44:922–929
53. Smith WC, Goldsmith TH (1991) The role of retinal photoisomerase in the visual cycle of the honeybee. J Gen Physiol 97:143–165
54. Spear PA, Boily M, Giroux I, DeBlois C, Leclair MH, Levasseur M, Leclair R (2009) Study design, water quality, morphometrics and age of the bullfrog, Rana catesbeiana, in sub-watersheds of the Yamaska River drainage basin, Québec, Canada. Aquat Toxicol 91:110–117
55. Tapparo A, Giorio C, Marzaro M, Marton D, Sold L, Girolami V (2011) Rapid analysis of neonicotinoid insecticides in guttation drops of corn seedlings obtained from coated seeds. J Environ Monit 13:1564–1568
56. Thornton BJ, Elthon TE, Cerny RL, Siegfried BD (2010) Proteomic analysis of atrazine exposure in Drosophila melanogaster (Diptera: Drosophilidae). Chemosphere 81:235–241
57. von Lintig J (2012) Metabolism of carotenoids and retinoids related to vision. J Biol Chem 287:1627–1634. doi:10.1074/jbc.R111.303990
58. von Lintig J, Dreher A, Kiefer C, Wernet M, Vogt K (2001) Analysis of the blind Drosophila mutant ninaB identifies the gene encoding the key enzyme for vitamin A formation in vivo. PNAS 98:1130–1135. doi:10.1073/pnas.031576398
59. Wang T, Jiao Y, Montell C (2007) Dissection of the pathway required for génération of vitamin A and for Drosophila phototransduction. J Cell Biol 177:305–316
60. Waris G, Ahsan H (2006) Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinogen 5:14
61. Weirich GF, Collins AM, Williams VP (2002) Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie 33:3–14
62. 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
63. Yang EC, Chuang YC, Chen YL, Chang LH (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 101:1743–1748