Antioxidant Enzymes of Honeybee Larvae Exposed to Oxamyl

M. Prezenská 1 , A. Sobeková 1 , and L. Sabová 2
  • 1 Institute of medical chemistry, University of Veterinary Medicine and Pharmacy in Košice, 041 81, Košice, Slovakia
  • 2 Institute of pharmacology, University of Veterinary Medicine and Pharmacy in Košice, 041 81, Košice, Slovakia

Abstract

Oxamyl is a carbamate insecticide used to control a broad spectrum of insects. It can also affect non-targeted organisms when applied incorrectly. The world food production depends partially on honeybee pollination abilities and therefore it is directly linked to the health of bees. The success of the colony development depends, among other factors, on the health of the larvae. The first 6 days are crucial for their development. In this stage, the worker larvae grow exponentially and may be exposed to xenobiotics via their diet. In this study, we investigated the effect of oxamyl on honeybee larvae (Apis mellifera) by monitoring the changes in their antioxidant enzyme system. The activities of superoxide dismutase, catalase and glutathione-S-transferase were determined in the homogenates of in vitro reared honeybee larvae after their single dietary exposure to oxamyl at doses of 1.25, 2.5, 5, 10 and 20 µg a.i./larva (a. i.—active ingredient). The doses of oxamyl did not cause statistically significant changes in the activities of the enzymes. Even a slight activation of these enzymes protected the larvae from the adverse effects of the reactive oxygen species (ROS). Marked changes in both the enzyme activity and the content of lipid peroxidation products were observed at the oxamyl dose of 10 µg a. i./larva. This fact may indicate a potential oxidative damage to the larvae. These results allowed us to assume that the toxic effects of oxamyl involves not only the inhibition of acetylcholine esterase but is also associated with ROS production.

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  • 1. Arena, M., Sgolastra, F., 2014: A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology, 23, 324—334. DOI: 10.1007/s10646-014-1190-1.

  • 2. Aupinel, P., Fortini, D., Michaud, B., Marolleau, F., Tasei, J. N., Odoux, J. F., 2007: Toxicity of dimethoate and fenoxycarb to honey bee brood (Apis mellifera), using a new in vitro standardized feeding method. Pest Manag. Sci., 63, 1090—1094. DOI: 10.1002/ps.1446.

  • 3. Badiou-Bénéteau, A., Carvalho, S. M., Brunet, J. L., Carvalho, G. A., Buleté, A., Giroud, B., Belzunces, L. P., 2012: Development of biomarkers of exposure to xenobiotics in the honey bee Apis mellifera: Application to the systemic insecticide thiamethoxam. Ecotoxicol. Environ. Saf., 82, 22—31. DOI: 10.1016/j.ecoenv.2012.05.005

  • 4. Bradford, M. M., 1976: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248—254.

  • 5. Carvalho, S. M., Belzunces, L. P., Carvalho, G. A., Brunet, J. L., Badiou-Beneteau, A., 2013: Enzymatic biomarkers as tools to assess environmental quality: A case study of exposure of the honeybee Apis mellifera to insecticides. Environ. Toxicol. Chem., 32, 2117—2124. DOI: 10.1002/etc.2288.

  • 6. Corona, M., Robinson, G. E., 2006: Genes of the antioxidant system of the honey bee: annotation and phylogeny. Insect Mol. Biol., 15, 687—701. DOI: 10.1111/j.1365-2583.2006.00695.x

  • 7. du Rand, E. E., Smit, S., Beukes, M., Apostolides, Z., Pirk, C. W. W., Nicolson, S. W., 2015: Detoxication mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine. Sci. Rep., 5: 11779, 1—11. DOI: 10.1038/srep11779. https://www.nature.com/articles/srep11779.pdf. Accessed July 02, 2015.

  • 8. Flohé, L., Ötting, F., 1984: Superoxide dismutase assays. Methods Enzymol., 105, 93—104.

  • 9. Genersch, E., 2010: Honey bee pathology: current threats to honey bees and beekeeping. Appl. Microbiol. Biotechnol., 87, 87—97. DOI: 10.1007/s00253-010-2573-8.

  • 10. Gutteridge, J. M. C., 1984: Ferrous ion-EDTA-stimulated phospholipid peroxidation. Biochem. J., 224, 697—701.

  • 11. Habig, W. H., Jakoby, W. B., 1981: Assays for differentiation of glutathione-S-transferases. Methods Enzymol., 77, 398— 405.

  • 12. Herbert, L. T., Vázquez, D. E., Arenas, A., Farina, W. M., 2014: Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour. J. Exp. Biol., 217, 3457—3464. DOI: 10.1242/jeb.109520.

  • 13. Hrassnigg, N., Crailsheim, K., 2005: Differences in drone and worker physiology in honeybees (Apis mellifera). Apidologie, 36, 255—277. DOI: 10.1051/apido:2005015.

  • 14. Human, H., Archer, C. R., du Rand, E. E., Pirk, C. W. W., Nicolson, S. W., 2014: Resistance of developing honeybee larvae during chronic exposure to dietary nicotine. J. Insect Physiol., 69, 74—79.

  • 15. Korayem, A. M., Khodairy, M. M., Abdel-Aal, A-A. A., El-Sonbaty, A. A. M., 2012: The protective strategy of antioxidant enzymes against hydrogen peroxide in honey bee, Apis mellifera during two different seasons. J. Biol. Earth Sci., 2, B93—B109.

  • 16. Manning, P., Ramanaidu, K., Cutler, G. C., 2017: Honey bee survival is affected by interactions between field-relevant rates of fungicides and insecticides used in apple and blueberry production. FACETS, 2, 910—918. DOI: 10.1139/facets-2017-0025.

  • 17. Milatovic, D., Gupta, R. C., Aschner, M., 2006: Anticholinesterase toxicity and oxidative stress. Sci. World J., 6, 295—310. DOI: 10.1100/tsw.2006.38.

  • 18. OECD. Guideline for the testing of chemicals No. 237. Honey bees (Apis mellifera) larval toxicity test, single exposure, section 2: Effects on biotic systems. 2013 https://www.oecdilibrary.org/docserver/9789264203723en.pdf?expires=1553171908&id=id&accname=guest&checksum=15822A5641 F332A2A0E4F3B79BA34 73C. Accessed March 15, 2019.

  • 19. Oliveira, R. A., Roat, T. C., Carvalho, S. M., Malaspina, O., 2014: Side-effects of thiamethoxam on the brain and midgut of the Africanized honeybee Apis mellifera (Hymenopptera: Apidae). Environ. Toxicol., 29, 1122—1133. DOI: 10.1002/tox.21842.

  • 20. Papadopoulos, A. I., Polemitou. I., Laifi, P., Yiangou, A., Tananaki. C., 2004: Glutathione S-transferase in the developmental stages of the insect Apis mellifera macedonica. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 139, 87—92. DOI:10.1016/j.cca.2004.09.009.

  • 21. Porrini, C., Sabatini, A. G., Girotti, S., Ghini, S., Medrzycki, P., Grillenzoni, F., et al., 2003: Honey bees and bee products as monitors of the environmental contamination. Apiacta, 38, 63—70.

  • 22. Sizer, I. W., Beers Jr., R. F., 1952: A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem., 195, 133—139.

  • 23. Sobeková, A., Holovská, K., Lenártová, V., Flešárová, S. Javorský, P., 2009: Another toxic effect of carbamate insecticides. Acta Biol. Hung., 60, 45—54. DOI: 10.1556/ABiol.60.2009.1.5.

  • 24. Tan, K., Yang, S., Wang, Z., Menzel, R., 2013: Effect of flumethrin on survival and olfactory learning in honeybees. PLoS One, 8. DOI: 10.1371/journal.pone.0066295. Accessed January 10, 2019.

  • 25. Weirich, G., Collins, A., Williams, V., 2002: Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie, 33, 3—14. DOI: 10.1051/apido:2001001.

  • 26. Yang, E.-C., Chang, H.-C., Wu, W.-Y., Chen, Y.-W., 2012: Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS One, 7. DOI: 10.1371/journal.pone.0049472. Accessed June 10, 2019.

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