The Impact of Pesticides on the Antioxidant System of Apis Mellifera Bees - A Systematic Review

Authors

  • Iloran R. C. Moreira College of Veterinary Medicine and Animal Sciences, UNESP, São Paulo State University, Botucatu, Brazil
  • Guilherme Duarte F. Souza College of Veterinary Medicine and Animal Sciences, UNESP, São Paulo State University, Botucatu, Brazil
  • Aline Astolfi College of Veterinary Medicine and Animal Sciences, UNESP, São Paulo State University, Botucatu, Brazil
  • Isabella Cristina de Castro Lippi College of Veterinary Medicine and Animal Sciences, UNESP, São Paulo State University, Botucatu, Brazil
  • Jaine L. Scheffer College of Veterinary Medicine and Animal Sciences, UNESP, São Paulo State University, Botucatu, Brazil
  • Renato Agostinho Arruda College of Veterinary Medicine and Animal Sciences, UNESP, São Paulo State University, Botucatu, Brazil
  • Suellen Matos da Silva College of Veterinary Medicine and Animal Sciences, UNESP, São Paulo State University, Botucatu, Brazil
  • Ricardo de Oliveira Orsi College of Veterinary Medicine and Animal Sciences, São Paulo State University, Botucatu-SP, Brazil

DOI:

https://doi.org/10.13102/sociobiology.v72i3.10894

Keywords:

Honeybees, foranging, free radicals

Abstract

During foraging, bees come into contact with different pesticides when collecting crop resources, affecting not only the bees but also the entire colony, resulting in damage to the antioxidant and immune system and a reduction in the number of individuals in the colony. An efficient antioxidant system is essential for bees due to their high metabolic rate, which produces significant free radicals under physiological conditions. Antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), and glutathione S-transferase (GST) are essential for combating oxidative stress. To better understand these effects, we adopted a systematic approach to review existing research on the potential impacts of pesticides on the antioxidant system of honey bees. Therefore, this review aims to list the papers published between 2020-2023 and show the effects of pesticides (insecticides, herbicides, and fungicides) on the antioxidant system of honey bees, focusing on the enzymes CAT, SOD, and GST. A total of 19 articles were found that met the criteria of this review, of which approximately 89% of the experiments were conducted in the laboratory and only 11% in the field. All of the studies assessed the exposure of bees to pesticides through ingestion, highlighting the lack of studies using the contact exposure method and conducting experiments in the field. It was, therefore, possible to suggest several points for future research to improve the current knowledge base on the potential effects of pesticides on honey bees.

Downloads

Download data is not yet available.

References

Al-Dalaen, S.M. & Al-Qtaitat, A.I. (2014). Review article: oxidative stress versus antioxidants. American Journal of Bioscience and Bioengineering, 2:60-71.

Almasri, H., Tavares, D.A., Pioz, M., Sené, D., Tchamitchian, S., Cousin, M., Brunet, J.C. & Belzunces, L.P. (2020). Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees. Ecotoxicology and Environmental Safety, 203: 111013.

Araújo, R.D.S., Lopes, M.P., Viana, T.A., Bastos, D.S.S., Machado-Neves, M., Botina, L.L. & Martins, G.F. (2023). Bioinsecticide spinosad poses multiple harmful effects on foragers of Apis mellifera. Environmental Science and Pollution Research, 30: 66923-66935.

Artz, D.R. & Pitts-Singer, T.L. (2015). Effects of fungicide and adjuvant sprays on nesting behavior in two managed solitary bees, Osmia lignaria and Megachile rotundata. PloS One, 10: e0135688.

Astolfi, A., Kadri, S.M., De Castro Lippi, I.C., Mendes, D.D., Alonso, D.P., Ribolla, P.E.M. & De Oliveira Orsi, R. (2022). Field relevant doses of the fipronil affects gene expression in honey bees Apis mellifera. Apidologie, 53: 69.

Barboza, H.T.G., Do Nascimento, X.P., Silva, O.F., Soares, A.G. & Dacosta, J B. (2018). Organophosphorus compounds and their role in agriculture. Revista Virtual de Quimica, 10: 172-193.

Bartling, M.T., Thümecke, S., Russert, J.H., Vilcinskas, A. & Lee, K.Z. (2021). Exposure to low doses of pesticides induces an immune response and the production of nitric oxide in honeybees. Scientific Reports, 11: 6819.

Basualdo, M., Cavigliasso, P., De Avila Jr, R.S., Aldea-Sánchez, P., Correa-Benítez, A., Harms, J.M., Ramos, A.K., Rojas-Bravo, V. & Salvarrey, S. (2022). Current status and economic value of insect-pollinated dependent crops in Latin America. Ecological Economics, 196: 107395.

Benito-Murcia, M., Botías, C., Martín-Hernández, R., Higes, M., Soler, F., Perez-Lopez, M., Míguez-Santiyán, M.P.M. & Martinez-Morcillo, S. (2022). Evaluating the chronic effect of two varroacides using multiple biomarkers and an integrated biological response index. Environmental Toxicology and Pharmacology, 94: 103920.

Bernauer, O.M., Gaines-Day, H.R., Steffan, S.A. (2015). Colonies of bumble bees (Bombus impatiens) produce fewer workers, less bee biomass, and have smaller mother queens following fungicide exposure. Insects, 6: 478-488.

Bovi, T.S., Zaluski, R. & Orsi, R.O. (2018). Toxicity and motor changes in Africanized honey bees (Apis mellifera L.) exposed to fipronil and imidacloprid. Anais da Academia Brasileira de Ciências, 90: 239-245.

Boyle, N.K., Pitts-Singer, T.L., Abbott, J., Alix, A., Cox-Foster, D.L., Hinarejos, S., Lehmann, D.M., Morandin, L., O’neil, B., Raine, N.E., Singh, R.; Thompson, H.M., Williams, N.M. & Steeger, T. (2019). Workshop on pesticide exposure assessment paradigm for non-Apis bees: foundation and summaries. Environmental Entomology, 48: 4-11.

Camilli, M.P., Kadri, S.M., Alvarez, M.V.N., Ribolla, P.E.M. & Orsi, R.O. (2022). Zinc supplementation modifies brain tissue transcriptome of Apis mellifera honeybees. BMC Genomics, 23: 282.

Candy, D.J., Becker, A. & Wegener, G. (1997). Coordination and integration of metabolism in insect flight. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 117: 497-512.

Cang, T., Lou, Y., Zhu, Y. C., Li, W., Weng, H.L.V.L. & Wang, Y. (2023). Mixture toxicities of tetrachlorantraniliprole and tebuconazole to honey bees (Apis mellifera L.) and the potential mechanism. Environment International, 172: 107764.

Chen, Y.Z., Zhang, B.W., Yang, J., Zou, C.S., Li, T., Zhang, G.C. & Chen, G.S. (2021). Detoxification, antioxidant, and digestive enzyme activities and gene expression analysis of Lymantria dispar larvae under carvacrol. Journal of Asia-Pacific Entomology, 24: 208-216.

Chmiel, J.A., Daisley, B.A., Pitek, A.P., Thompson, G.J. & Reid, G. (2020). Understanding the effects of sublethal pesticide exposure on honey bees: a role for probiotics as mediators of environmental stress. Frontiers in Ecology and Evolution, 8: 22.

Christen, V., Mittner, F. & Fent, K. (2016). Molecular effects of neonicotinoids in honey bees (Apis mellifera). Environmental Science and Technology, 50: 4071-4081.

Christen, V. & Fent, K. (2017). Exposure of honey bees (Apis mellifera) to different classes of insecticides exhibit distinct molecular effect patterns at concentrations that mimic environmental contamination. Environmental Pollution, 226: 48-59.

Christen, V., Kunz, P.Y. & Fent, K. (2018). Endocrine disruption and chronic effects of plant protection products in bees: Can we better protect our pollinators?. Environmental Pollution, 243: 1588-1601.

Clarke, J. (2011). What is a systematic review?. Evidence-Based Nursing, 14: 64-64.

Colin, T., Meikle, W.G., Wu, X. & Barron, A.B. (2019). Traces of a neonicotinoid induce precocious foraging and reduce foraging performance in honey bees. Environmental Science and Technology, 53: 8252-8261.

Corona, M. & Robinson, G.E. (2006). Genes of the antioxidant system of the honey bee: annotation and phylogeny. Insect Molecular Biology, 15: 687-701.

Cullen, M.G., Thompson, L.J., Carolan, J.C., Stout, J.C. & Stanley, D.A. (2019). Fungicides, herbicides and bees: A systematic review of existing research and methods. PLoS One, 14: e0225743.

Dai, P., Jack, C.J., Mortensen, A.N., Bloomquist, J.R. & Ellis, J.D. (2018). The impacts of chlorothalonil and diflubenzuron on Apis mellifera L. larvae reared in vitro. Ecotoxicology and Environmental Safety, 164: 283-288.

De Almeida Rossi, C., Roat, T.C., Tavares, D.A., Cintra-Socolowski, P. & Malaspina, O. (2013). Brain morphophysiology of Africanized bee Apis mellifera exposed to sublethal doses of imidacloprid. Archives of Environmental Contamination and Toxicology, 65: 234-243.

Decio, P., Miotelo, L., Pereira, F.D.C.; Roat, T.C., Marin-Morales, M.A. & Malaspina, O. (2021). Enzymatic responses in the head and midgut of Africanized Apis mellifera contaminated with a sublethal concentration of thiamethoxam. Ecotoxicology and Environmental Safety, 223: 112581.

De Oliveira, D.M., Agostinetto, L. & Siegloch, A.E. (2023). Comparison of the drinking water standard for pesticides of the Brazil with other countries. Heliyon, 9: e13783 .

Domingues, C.E., Abdalla, F.C., Balsamo, P.J., Pereira, B.V., De Alencar Hausen, M., Costa, M.J. & Silva-Zacarin, E.C. (2017). Thiamethoxam and picoxystrobin reduce the survival and overload the hepato-nephrocitic system of the Africanized honeybee. Chemosphere, 186: 994-1005.

Dos Santos, C.F., Acosta, A.L., Dorneles, A.L., Dos Santos, P.D. & Blochtein, B. (2016). Queens become workers: pesticides alter caste differentiation in bees. Scientific Reports, 6: 31605.

Dulin, F., Zatylny-Gaudin, C., Ballandonne, C., Guillet, B., Bonafos, R., Bureau, R. & Halm, M.P. (2014). Protecting honey bees: identification of a new varroacide by in silico, in vitro, and in vivo studies. Parasitology Research, 113: 4601-4610.

Dziechciarz, P., Strachecka, A., Borsuk, G. & Olszewski, K. (2023). Effect of rearing in small-cell combs on activities of catalase and superoxide dismutase and total antioxidant capacity in the hemolymph of Apis mellifera workers. Antioxidants, 12: 709.

Favaro, R., Bauer, L.M., Rossi, M., D’ambrosio, L.; Bucher, E. & Angeli, S. (2019). Botanical origin of pesticide residues in pollen loads collected by honeybees during and after apple bloom. Frontiers in Physiology, 10: 1069.

Feazel-Orr, H.K., Caltalfamo, K.M., Brewster, C.C., Fell, R.D., Anderson, T.D. & Traver, B.E. (2016). Effects of pesticide treatments on nutrient levels in worker honey bees (Apis mellifera). Insects, 7: 8.

Feketéné Ferenczi, A., Szűcs, I. & Bauerné Gáthy, A. (2023). Evaluation of the Pollination Ecosystem Service of the Honey Bee (Apis mellifera) Based on a Beekeeping Model in Hungary. Sustainability, 15: 9906.

Fisher, A. & Rangel, J. (2018). Exposure to pesticides during development negatively affects honey bee (Apis mellifera) drone sperm viability. PLoS One, 13: e0208630.

Fisher, A., Coleman, C., Hoffmann, C., Fritz, B. & Rangel, J. (2017). The synergistic effects of almond protection fungicides on honey bee (Hymenoptera: Apidae) forager survival. Journal of Economic Entomology, 110: 802-808.

Fischer, J., Müller, T., Spatz, A.K., Greggers, U., Grünewald, B. & Menzel, R. (2014). Neonicotinoids interfere with specific components of navigation in honeybees. PloS One, 9: e91364.

Florencia, F.M., Carolina, T., Enzo, B. & Leonardo, G. (2017). Effects of the herbicide glyphosate on non-target plant native species from Chaco forest (Argentina). Ecotoxicology and Environmental Safety, 144: 360-368.

Freemark, K. & Boutin, C. (1995). Impacts of agricultural herbicide use on terrestrial wildlife in temperate landscapes: a review with special reference to North America. Agriculture, Ecosystems and Environment, 52: 67-91.

Galvão, T.F., Pansani, T.S.A. & Harrad, D. (2015). Principais itens para relatar Revisões sistemáticas e Meta-análises: A recomendação PRISMA. Epidemiologia e Serviços de Saúde,

: 335-342.

Gao, J., Yang, Y., Ma, S., Liu, F., Wang, Q., Wang, X., Wu, Y., Zhang, L., Liu, Y., Diao, Q. & Dai, P. (2022). Combined transcriptome and metabolite profiling analyses provide insights into the chronic toxicity of carbaryl and acetamiprid to Apis mellifera larvae. Scientific Reports, 12: 16898.

Giglio, A. & Vommaro, M.L. (2022). Dinitroaniline herbicides: a comprehensive review of toxicity and side effects on animal non-target organisms. Environmental Science and Pollution Research, 29: 76687-76711.

Goulson, D., Nicholls, E., Botías, C. & Rotheray, E.L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347: 1255957.

Gunstone, T., Cornelisse, T., Klein, K., Dubey, A. & Donley, N. (2021). Pesticides and soil invertebrates: A hazard assessment. Frontiers in Environmental Science, 9: 122.

Halliwell, B. (2007). Oxidative stress and cancer: have we moved forward? Biochemical Journal, 401: 1-11.

Han, W., Yang, Y., Gao, J., Zhao, D., Ren, C., Wang, S., Zhao, S. & Zhong, Y. (2019). Chronic toxicity and biochemical response of Apis cerana cerana (Hymenoptera: Apidae) exposed to acetamiprid and propiconazole alone or combined. Ecotoxicology, 28: 399-411.

He, B., Liu, Z., Wang, Y., Cheng, L., Qing, Q., Duan, J., Xu, J., Dang, X., Zhou, Z. & Li, Z. (2021). Imidacloprid activates ROS and causes mortality in honey bees (Apis mellifera) by inducing iron overload. Ecotoxicology and Environmental Safety, 228: 112709.

Henry, M., Cerrutti, N., Aupinel, P., Decourtye, A., Gayrard, M., Odoux, J.F., Pissard, A. & Bretagnolle, V. (2015). Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees. Proceedings of the Royal Society B: Biological Sciences, 282:20152110.

Ibrahim, E.D.S., Abd Alla, A.E., El-Masarawy, M.S., Salem, R.A., Hassan, N.N. & Moustafa, M.A. (2023). Sulfoxaflor influences the biochemical and histological changes on honeybees (Apis mellifera L.). Ecotoxicology, 32: 674-681.

Jiang, J., Ma, D., Zou, N., Yu, X., Zhang, Z., Liu, F. & Mu, W. (2018). Concentrations of imidacloprid and thiamethoxam in pollen, nectar and leaves from seed-dressed cotton crops and their potential risk to honeybees (Apis mellifera L.). Chemosphere, 201: 159-167.

Johnson, R.M. (2015). Honey bee toxicology. Annual Review of Entomology, 60: 415-434.

Kodrík, D., Bednářová, A., Zemanová, M. & Krishnan, N. (2015). Hormonal regulation of response to oxidative stress in insects - an update. International Journal of Molecular Sciences, 16: 25788-25816.

Korenko, S., Niedobová, J., Kolářová, M., Hamouzová, K., Kysilková, K. & Michalko, R. (2016). The effect of eight common herbicides on the predatory activity of the agrobiont spider Pardosa agrestis. BioControl, 61: 507-517.

Kraus, E.C. & Stout, M.J. (2019). Direct and indirect effects of herbicides on insect herbivores in rice, Oryza sativa. Scientific Reports, 9: 6998.

Krupke, C.H., Hunt, G.J., Eitzer, B.D., Andino, G. & Given, K. (2012). Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One, 7: e29268.

Leska, A., Nowak, A., Nowak, I. & Górczyńska, A. (2021). Effects of insecticides and microbiological contaminants on Apis mellifera health. Molecules, 26: 5080.

Lewis, K.A., Tzilivakis, J., Warner, D.J. & Green, A. (2016). An international database for pesticide risk assessments and management. Human and Ecological Risk Assessment: An International Journal, 22: 1050-1064.

Li, Z., Yu, T., Chen, Y., Heerman, M., He, J., Huang, J., Nie, H. & Su, S. (2019). Brain transcriptome of honey bees (Apis mellifera) exhibiting impaired olfactory learning induced by a sublethal dose of imidacloprid. Pesticide Biochemistry and Physiology, 156: 36-43.

Li, J., Zhao, L., Qi, S., Zhao, W., Xue, X., Wu, L. & Huang, S. (2021). Sublethal effects of Isoclast™ Active (50% sulfoxaflor water dispersible granules) on larval and adult worker honey bees (Apis mellifera L.). Ecotoxicology and Environmental Safety, 220: 112379.

Li, Z., Duan, J., Chen, L., Wang, Y., Qin, Q., Dang, X. & Zhou, Z. (2022). Melatonin enhances the antioxidant capacity to rescue the honey bee Apis mellifera from the ecotoxicological effects caused by environmental imidacloprid. Ecotoxicology and Environmental Safety, 239: 113622.

Lima, M.A.P., Martins, G.F., Oliveira, E.E. & Guedes, R.N.C.

(2016). Agrochemical-induced stress in stingless bees: peculiarities, underlying basis, and challenges. Journal of Comparative Physiology A, 202: 733-747.

Lundin, O., Rundlöf, M., Smith, H.G., Fries, I. & Bommarco, R. (2015). Neonicotinoid insecticides and their impacts on bees: a systematic review of research approaches and identification of knowledge gaps. PLoS One, 10: e0136928.

Main, A.R., Hladik, M.L., Webb, E.B., Goyne, K.W. & Mengel, D. (2020). Beyond neonicotinoids-wild pollinators are exposed to a range of pesticides while foraging in agroecosystems. Science of the Total Environment, 742: 140436.

Michalková, V. & Pekár, S. (2009). How glyphosate altered the behaviour of agrobiont spiders (Araneae: Lycosidae) and beetles (Coleoptera: Carabidae). Biological Control, 51: 444-449.

Migdał, P., Murawska, A., Strachecka, A., Bieńkowski, P. & Roman, A. (2020). Changes in the honeybee antioxidant system after 12 h of exposure to electromagnetic field frequency of 50 hz and variable intensity. Insects, 11: 713.

Gomes, N.I., Castelan, I.V.K., Gontijo, M.L. & Resende, C.H. (2020). Honeybee survival and flight capacity are compromised by insecticides used for controlling melon pests in Brazil. Ecotoxicology, 29: 97-107.

Nettles, R., Watkins, J., Ricks, K., Boyer, M., Licht, M., Atwood, L.W., Peoples, M., Smith, R.G., Mortensen, D.A. & Koide, R.T. (2016). Influence of pesticide seed treatments on rhizosphere fungal and bacterial communities and leaf fungal endophyte communities in maize and soybean. Applied Soil Ecology, 102: 61-69.

Niemeyer, J.C., De Santo, F.B., Guerra, N., Ricardo Filho, A.M. & Pech, T.M. (2018). Do recommended doses of glyphosate-based herbicides affect soil invertebrates? Field and laboratory screening tests to risk assessment. Chemosphere, 198: 154-160.

Nikolić, T.V., Kojić, D., Orčić, S., Batinić, D., Vukašinović, E., Blagojević, D.P. & Purać, J. (2016). The impact of sublethal concentrations of Cu, Pb, and Cd on honey bee redox status, superoxide dismutase, and catalase in laboratory conditions. Chemosphere, 164: 98-105.

Olgun, T., Dayioğlu, M., & Özsoy, N. (2020). Pesticide and pathogen induced oxidative stress in honey bees (Apis mellifera L.). Mellifera, 20:32-52.

Orčić, S.M., Čelić, T.V., Purać, J.S., Vukašinović, E.L. & Kojić, D.K. (2022). Acute toxicity of sublethal concentrations of thiacloprid and clothianidin to immune response and oxidative status of honey bees. Apidologie, 53: 50.

Pal, E., Almasri, H., Paris, L., Diogon, M., Pioz, M., Cousin, M., Sené, D., Tchamitchian, S., Tavares, D.A., Delbac, F., Blot, N., Brunet, J.L. & Belzunces, L.P. (2022). Toxicity of the pesticides imidacloprid, difenoconazole and glyphosate alone and in binary and ternary mixtures to winter honey bees: effects on survival and antioxidative defenses. Toxics, 10: 104.

Paleolog, J., Wilde, J., Miszczak, A., Gancarz, M. & Strachecka, A. (2021). Antioxidation defenses of Apis mellifera queens and workers respond to imidacloprid in different age-dependent ways: Old queens are resistant, foragers are not. Animals, 11: 1246.

Parkinson, R.H., Fecher, C. & Gray, J.R. (2022). Chronic exposure to insecticides impairs honeybee optomotor behaviour. Frontiers in Insect Science, 2: 936826.

Pleasants, J.M. & Oberhauser, K.S. (2013). Milkweed loss in agricultural fields because of herbicide use: effect on the monarch butterfly population. Insect Conservation and Diversity, 6: 135-144.

Pons, D.G., Herrera, C., Torrens-Mas, M., Leza, M. & Sastre-Serra, J. (2023). Sublethal doses of glyphosate modulate mitochondria and oxidative stress in honeybees by direct feeding. Archives of Insect Biochemistry and Physiology, 114: e22028.

Prosser, R.S., Anderson, J.C., Hanson, M.L., Solomon, K.R. & Sibley, P.K. (2016). Indirect effects of herbicides on biota in terrestrial edge-of-field habitats: A critical review of the literature. Agriculture, Ecosystems and Environment, 232: 59-72.

Qi, S., Niu, X., Hui Wang, D., Wang, C., Zhu, L., Xue, X., Zhang, Z. & Wu, L. (2020). Flumethrin at sublethal concentrations induces stresses in adult honey bees (Apis mellifera L.). Science of the Total Environment, 700: 134500.

Rondeau, S. & Raine, N.E. (2022). Fungicides and bees: a review of exposure and risk. Environment International, 165: 107311.

Russo, L., Buckley, Y.M., Hamilton, H., Kavanagh, M., & Stout, J.C. (2020). Low concentrations of fertilizer and herbicide alter plant growth and interactions with flower-visiting insects. Agriculture, Ecosystems and Environment, 304: 107141.

Sagona, S., Betti, L., Casini, L., Palego, L., Giannaccini, G. & Felicioli, A. (2021). Antioxidant enzymes activity during age polyethism in Apis mellifera L., 1758. Journal of Apicultural Research, 60: 879-889.

Sánchez-Moreno, S., Castro, J., Alonso-Prados, E., Alonso-Prados, J.L., García-Baudín, J.M., Talavera, M. & Durán-Zuazo, V.H. (2015). Tillage and herbicides decrease soil biodiversity in olive orchards. Agronomy for Sustainable Development, 35: 691-700.

Sharma, A., Jha, P. & Gadi V.P.R. (2018). Multidimensional relationships of herbicides with insect-crop food webs. Science of the Total Environment, 643: 1522-1532.

Stellin, F., Gavinelli, F., Stevanato, P., Concheri, G., Squartini, A. & Paoletti, M.G. (2018). Effects of different concentrations of glyphosate (Roundup 360®) on earthworms (Octodrilus complanatus, Lumbricus terrestris, and Aporrectodea caliginosa) in vineyards in the North-East of Italy. Applied Soil Ecology, 123: 802-808.

Tan, K., Chen, W., Dong, S., Liu, X., Wang, Y. & Nieh, J.C. (2015). A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Scientific Reports, 5: 10989.

Tawfik, A.I., Ahmed, Z.H., Abdel-Rahman, M.F. & Moustafa, A.M. (2020). Influence of winter feeding on colony development and the antioxidant system of the honey bee, Apis mellifera. Journal of Apicultural Research, 59: 752-763.

Thanomsit, C., Saowakoon, S., Wattanakornsiri, A., Nanuam, J., Prasatkaew, W., Nanthanawat, P., Mongkolvai, P. & Chalorcharoenying, W. (2020). The glyphosate (Roundup): fate in aquatic environment, adverse effect and toxicity assessment in aquatic organisms. Naresuan University Journal: Science and Technology (NUJST), 28: 65-81.

Traynor, K.S. & Lamas, Z.S. (2021). Social disruption: Sublethal pesticides in pollen lead to Apis mellifera queen events and brood loss. Ecotoxicology and Environmental Safety, 214: 112105.

Todd, O.E., Figueiredo, M.R., Morran, S., Soni, N., Preston, C., Kubeš, M.F., Napier, R. & Gaines, T.A. (2020). Synthetic auxin herbicides: finding the lock and key to weed resistance. Plant Science, 300: 110631.

Tosi, S., Burgio, G. & Nieh, J.C. (2017). A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Scientific Reports, 7: 1201.

Tosi, S. & Nieh, J.C. (2017). A common neonicotinoid pesticide, thiamethoxam, alters honey bee activity, motor functions, and movement to light. Scientific Reports, 7: 15132.

Sanchez-Bayo, F. & Goka, K. (2016). Impacts of pesticides on honey bees. Beekeeping and Bee Conservation-Advances in Research, 4: 77-97.

Sharma, A., Jha, P. & Reddy, G.V.P. (2018). Multidimensional relationships of herbicides with insect-crop food webs. Science of the Total Environment, 643: 1522-1532.

Wang, H., Lu, Z., Li, M., Fang, Y., Qu, J., Mao, T., Chen, J., Li, F., Sun, H. & Li, B. (2020). Responses of detoxification enzymes in the midgut of Bombyx mori after exposure to low-dose of acetamiprid. Chemosphere, 251: 126438.

Wang, D., Lv, L., Gao, Z., Zhu, Y. C., Weng, H., Yang, G. & Wang, Y. (2023). Joint toxic effects of thiamethoxam and flusilazole on the adult worker honey bees (Apis mellifera L.). Environmental Pollution, 317: 120806.

Wu, J., Ge, L., Liu, F., Song, Q. & Stanley, D. (2020). Pesticide-induced planthopper population resurgence in rice cropping systems. Annual Review of Entomology, 65: 409-429.

Wu, X., Liao, C., He, X., Zhang, L., Yan, W. & Zeng, Z. (2022). Sublethal fluvalinate negatively affects the development and flight capacity of honeybee (Apis mellifera L.) workers. Environmental Research, 203: 111836.

Zaluski, R., Kadri, S.M., Alonso, D.P., Robolla, P.E.M. & Orsi, R.O. (2015). Fipronil promotes motor and behavioral changes in honey bees (Apis mellifera) and affects the development of colonies exposed to sublethal doses. Environmental Toxicology and Chemistry, 34: 1062-1069.

Zaluski, R., Justulin Jr, L.A. & Orsi, R.O. (2017). Field-relevant doses of the systemic insecticide fipronil and fungicide pyraclostrobin impair mandibular and hypopharyngeal glands in nurse honeybees (Apis mellifera). Scientific Reports, 7: 15217.

Zaluski, R., Bittarello, A.C., Vieira, J.C.S., Braga, C.P., Padilha, P.D.M., Fernandes, M.D.S., Bovi, S.T. & Orsi, R.O. (2020). Modification of the head proteome of nurse honeybees (Apis mellifera) exposed to field-relevant doses of pesticides. Scientific Reports, 10: 2190.

Zhao, H., Li, G., Guo, D., Wang, Y., Liu, Q., Gao, Z., Whang, H., Liu, Z., Gou, X. & Xu, B. (2020). Transcriptomic and metabolomic landscape of the molecular effects of glyphosate commercial formulation on Apis mellifera ligustica and Apis cerana cerana. Science of The Total Environment, 744: 140819.

Zhao, H., Li, G., Cui, X., Wang, H., Liu, Z., Yang, Y. & Xu, B. (2022). Review on the effects of some insecticides on honey bee health. Pesticide Biochemistry and Physiology, 188: 105219.

Zou, C., Lv, C., Wang, Y., Cao, C. & Zhang, G. (2017). Larvicidal activity and insecticidal mechanism of Chelidonium majus on Lymantria dispar. Pesticide Biochemistry and Physiology, 142: 123-132.

Zubrod, J.P., Bundschuh, M., Arts, G., Brühl, C.A., Imfeld, G., Knäbel, A., Payraudeau, S., Rasmussen, J.J., Rohr, J., Scharmuller, A., Smalling, K., Stehle, S., Schulz, R. & Schäfer, R.B. (2019). Fungicides: an overlooked pesticide class? Environmental Science & Technology, 53: 3347-3365.

Downloads

Published

2025-07-02

How to Cite

Moreira, I. R. C., Souza, G. D. F., Astolfi, A., Lippi, I. C. C., Scheffer, J. L., Arruda, R. A., Silva, S. M. da, & Orsi, R. de O. (2025). The Impact of Pesticides on the Antioxidant System of Apis Mellifera Bees - A Systematic Review. Sociobiology, 72(3), e10894. https://doi.org/10.13102/sociobiology.v72i3.10894

Issue

Section

Review

Most read articles by the same author(s)