Skip to main content
SpringerLink
Log in

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

  • Crop protection: environment, human health, and biodiversity
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The decline in the population of pollinators is a worrying phenomenon worldwide. In North America, the extensive use of herbicides in maize and soya crops may affect the health of nontarget organisms like the honey bee. In this study, caged honey bees were exposed to realistic doses of atrazine, metolachlor, and glyphosate for 10 days via contaminated syrup. Peroxidation of lipids was evaluated using the thiobarbituric acid reactive substance (TBARS) test, and diet-derived antioxidants—carotenoids, all-trans-retinol (at-ROH) and α-tocopherol—were detected and quantified using reversed-phase HPLC techniques. Significant increases in syrup consumption were observed in honey bees exposed to metolachlor, and a lower TBARS value was recorded for the highest dose. No relationship was observed between the peroxidation of lipids and the levels of antioxidants. However, β-carotene, which was found to be the most abundant carotenoid, and at-ROH (derived from β-carotene) both decreased with increasing doses of atrazine and glyphosate. In contrast, metolachlor increased levels of at-ROH without any effects on β-carotene. These results show that the honey bee carotenoid–retinoid system may be altered by sublethal field-realistic doses of herbicides.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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

    Google Scholar 

  • ARLA (Agence de réglementation de la lutte antiparasitaire) (2007) Décision de réévaluation: atrazine (Évaluation environnementale). Santé Canada, Sécurité des produits de consommation, RVD2007-05

  • Arshavsky VY (2009) Vision: the retinoid cycle in Drosophila. Curr Biol R96–8. doi:10.1016/j.cub.2009.12.039

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Casani R (2000) Vitamin E. Kirk-Othmer encyclopedia of chemical technology. doi:10.1002/0471238961.2209200103011901.a01

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • George DGM, Gatehouse AMR (2013) Oxidative stress enzymes in Busseola fusca. Int J Curr Microbiol App Sci 2:485–495

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • Hahn DA, Denlinger DL (2007) Meeting the energetic demands of insect diapause: nutrient storage and utilization. J Insect Physiol 53:760–773

    Article  CAS  Google Scholar 

  • Halme A, Cheng M, Hariharan IK (2010) Retinoids regulate a developmental checkpoint for tissue regeneration in Drosophila. Curr Biol 20:458–463

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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)

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity. Apidologie 41:312–332

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kayser H (1982) Carotenoids in insects. In: Britton G, Goodwin TW (eds) Carotenoid chemistry and biochemistry. Pergamon Press, Toronto, pp 195–210

    Chapter  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Maini S, Medrzycki P, Porrini C (2010) The puzzle of honey bee losses: a brief review. Bull Insectol 63:153–160

    Google Scholar 

  • Mueller L, Boehm V (2011) Antioxidant activity of β-carotene compounds in different in vitro assays. Molecules 16:1055–1069. doi:10.3390/molecules16021055

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ohkawa H, Ohishi N, Tagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Chem 95:351–358

    CAS  Google Scholar 

  • Otis GW, Wheeler DE, Buck N, Mattila HR (2004) Storage proteins in winter honey bees. Apiacata 38:352–357

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shete V, Quadro L (2013) Mammalian metabolism of β-Carotene: gaps in knowledge. Nutrients 5:4849–4868. doi:10.3390/nu5124849

    Article  CAS  Google Scholar 

  • Singh M, Sandhir R, Kiron R (2010) Alterations in Ca2+ homeostasis in rat erythrocytes with atrazine treatment: positive modulation by vitamin E. Mol Cell Biochem 340:231–238

    Article  CAS  Google Scholar 

  • Široká Z, Drastichová J (2004) Biochemical markers of aquatic environment contamination-cytochrome P450 in fish. A review. Acta Vet Brno 73:123–132

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Smith WC, Goldsmith TH (1991) The role of retinal photoisomerase in the visual cycle of the honeybee. J Gen Physiol 97:143–165

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Thornton BJ, Elthon TE, Cerny RL, Siegfried BD (2010) Proteomic analysis of atrazine exposure in Drosophila melanogaster (Diptera: Drosophilidae). Chemosphere 81:235–241

    Article  CAS  Google Scholar 

  • von Lintig J (2012) Metabolism of carotenoids and retinoids related to vision. J Biol Chem 287:1627–1634. doi:10.1074/jbc.R111.303990

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Waris G, Ahsan H (2006) Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinogen 5:14

    Article  Google Scholar 

  • Weirich GF, Collins AM, Williams VP (2002) Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie 33:3–14

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Maxime Gauthier for HPLC technical assistance. We also thank Dr. Diana Averill for generous advices in TBARS analysis. We are grateful to Dr. Philip Spear for providing access to his laboratory and TOXEN (Centre de recherche en toxicologie de l’environnement) for the use of analytical equipment. This study was supported by the Programme de soutien à l’innovation en agroalimentaire (PSIA) from Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec (MAPAQ), attributed to M. Boily (#811175).

Author information

Authors and Affiliations

  1. Département des Sciences Biologiques, Université du Québec à Montréal, C.P. 8888, Succursale Centre-Ville, Montréal, QC, H3C 3P8, Canada

    Stephanie Hedrei Helmer, Philippe Aras, Catherine Jumarie & Monique Boily

  2. Département des Sciences de l’Environnement, Université du Québec à Montréal, C.P. 8888, Succursale Centre-Ville, Montréal, QC, H3C 3P8, Canada

    Anahi Kerbaol

Authors
  1. Stephanie Hedrei Helmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anahi Kerbaol
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philippe Aras
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Catherine Jumarie
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Monique Boily
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Monique Boily.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 50 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Helmer, S.H., Kerbaol, A., Aras, P. et al. Effects of realistic doses of atrazine, metolachlor, and glyphosate on lipid peroxidation and diet-derived antioxidants in caged honey bees (Apis mellifera). Environ Sci Pollut Res 22, 8010–8021 (2015). https://doi.org/10.1007/s11356-014-2879-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-2879-7

Keywords

Search

Navigation