Acute Toxicity of Selected Insecticides on Apis mellifera and Ceratina smaragdula: Laboratory and Field Assessments
DOI:
https://doi.org/10.13102/sociobiology.v73i3.11980Keywords:
honey bee, solitary bee, pesticides, IPPMAbstract
Pollinators are vital to agricultural productivity, yet their populations are declining due to anthropogenic disturbances, including pesticide use. This study evaluated the acute toxicity of selected insecticides to two bee species, the honey bee (Apis mellifera) and the small carpenter bee (Ceratina smaragdula), using laboratory and field experiments. Under laboratory conditions, emamectin benzoate exhibited the highest toxicity to C. smaragdula, with a 12-hour LC₅₀ of 4.69 µg/mL. Moderate toxicity was observed for flubendiamide (LC₅₀ = 60.57 µg/mL) and chlorantraniliprole (LC₅₀ = 57.64 µg/mL), whereas the remaining insecticides showed higher LC₅₀ values ranging from 141.41 to 846.77 µg/mL. After 24 hours, emamectin benzoate remained the most toxic (LC₅₀ = 1.14 µg/mL), and similar toxicity patterns were observed for the other insecticides. In A. mellifera, emamectin benzoate was also the most toxic insecticide at both 12 hours (LC₅₀ = 9.64 µg/mL) and 24 hours (LC₅₀ = 5.10 µg/mL). Moderate toxicity was recorded for flubendiamide and chlorantraniliprole, while the other insecticides exhibited lower toxicity, with 24-hour LC₅₀ values ranging from 56.35 to 589.92 µg/mL. Field applications resulted in significant differences in bee abundance between treated and untreated plots, with the highest abundance in untreated plots and the lowest in bifenthrin-treated plots. Overall, bee abundance increased over time, peaking 72 hours after insecticide application. These findings highlight the need for further investigation into the long-term effects of pesticides, particularly on understudied solitary bee species across diverse ecosystems.
Downloads
References
Abdu-Allah, G.A.M. & Pittendrigh, B.R. (2018). Lethal and sub-lethal effects of select macrocyclic lactones insecticides on forager worker honey bees under laboratory experimental conditions. Ecotoxicology, 27: 81-88. DOI: https://doi.org/10.1007/s10646-017-1872-6
Abdullah, S., Ali, M., Khan, F. Z. A., Sajjad, A., Qayyum, M. A. & Ahmad, N. (2024). Solitary Bees Are More Efficient Pollinators of Sponge Gourd than Giant honeybees and Syrphid Flies. Sociobiology, 71: e10279. DOI: https://doi.org/10.13102/sociobiology.v71i3.10279
Ali, M., Saeed, S., Sajjad, A. & Whittington, A. (2011). In search of the best pollinators for canola (Brassica napus L.) production in Pakistan. Applied Entomology and Zoology, 46: 353-361. DOI: https://doi.org/10.1007/s13355-011-0051-0
Ali, Q., Ali, M., Khan, F. Z. A., Noureldeen, A., Alghamdi, A., Darwish, H., Fatima, A., Jalali, A. I., Prendergast, K. & Saeed, S. (2024). Water Deprivation and Sowing Times Alter Plant-Pollination Interactions and Seed Yield in Sunflower, Helianthus annuus L. (Asteraceae). Plants, 13: 3194. DOI: https://doi.org/10.3390/plants13223194
Anees, M., Ali, M., Ghramh, H. A., Sajjad, A., Ali Khan, K., Saeed, S. & Razzaq, K. (2022). Impact of Bee and Fly Pollination on Physical and Biochemical Properties of Strawberry Fruit. Horticulturae, 8: 1072. DOI: https://doi.org/10.3390/horticulturae8111072
Arena, M. & Sgolastra, F. (2014). A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology, 23: 324-334. DOI: https://doi.org/10.1007/s10646-014-1190-1
Badawy, M. E. I., Nasr, H. M. & Rabea, E. I. (2015). Toxicity and biochemical changes in the honey bee Apis mellifera exposed to four insecticides under laboratory conditions. Apidologie, 46: 177-193. DOI: https://doi.org/10.1007/s13592-014-0315-0
Bass, C., Denholm, I., Williamson, M. S. & Nauen, R. (2015). The global status of insect resistance to neonicotinoid insecticides. Pesticide Biochemistry and Physiology, 121: 78-87. DOI: https://doi.org/10.1016/j.pestbp.2015.04.004
Beadle, K., Singh, K. S., Troczka, B. J., Randall, E., Zaworra, M., Zimmer, C. T., Hayward, A., Reid, R., Kor, L., Kohler, M., Buer, B., Nelson, D. R., Williamson, M. S., Davies, T. G. E., Field, L. M., Nauen, R. & Bass, C. (2019). Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. PLOS Genetics, 15: e1007903. DOI: https://doi.org/10.1371/journal.pgen.1007903
Biondi, A., Mommaerts, V., Smagghe, G., Viñuela, E., Zappalà, L. & Desneux, N. (2012). The non‐target impact of spinosyns on beneficial arthropods. Pest Management Science, 68: 1523-1536. DOI: https://doi.org/10.1002/ps.3396
Boff, S., Scheiner, R., Raizer, J. & Lupi, D. (2021). Survival rate and changes in foraging performance of solitary bees exposed to a novel insecticide. Ecotoxicology and Environmental Safety, 211: 111869. DOI: https://doi.org/10.1016/j.ecoenv.2020.111869
Claudianos, C., Ranson, H., Johnson, R. M., Biswas, S., Schuler, M. A., Berenbaum, M. R., Feyereisen, R. & Oakeshott, J. G. (2006). A deficit of detoxification enzymes: Pesticide sensitivity and environmental response in the honeybee. Insect Molecular Biology, 15: 615-636. DOI: https://doi.org/10.1111/j.1365-2583.2006.00672.x
Dai, P.-L., Wang, Q., Sun, J.-H., Liu, F., Wang, X., Wu, Y.-Y. & Zhou, T. (2009). Effects of sublethal concentrations of bifenthrin and deltamethrin on fecundity, growth, and development of the honeybee Apis mellifera ligustica. Environmental Toxicology and Chemistry, 29: 644-649. DOI: https://doi.org/10.1002/etc.67
Delabie, J., Bos, C., Fonta, C. & Masson, C. (1985). Toxic and repellent effects of cypermethrin on the honeybee: Laboratory, glasshouse and field experiments. Pesticide Science, 16: 409-415. DOI: https://doi.org/10.1002/ps.2780160417
Devillers, J. & Devillers, H. (2020). Lethal and Sublethal Effects of Pyriproxyfen on Apis and Non-Apis Bees. Toxics, 8: 104. DOI: https://doi.org/10.3390/toxics8040104
Devkota, K., Dos Santos, C. F., Ferreira, A. B. & Timberlake, T. P. (2024). Assessing the economic and nutritional value of pollination services in Nepal. Scientific Reports, 14: 24037. DOI: https://doi.org/10.1038/s41598-024-75584-x
Egan, P.A., Dicks, L.V., Hokkanen, H M.T. & Stenberg, J.A. (2020). Delivering Integrated Pest and Pollinator Management (IPPM). Trends in Plant Science, 25: 577-589. DOI: https://doi.org/10.1016/j.tplants.2020.01.006
Ejaz, K., Ali, M., Khan, F. Z. A. & Mozūratis, R. (2025). Enhancing Alfalfa (Medicago sativa) Seed Yield: The Effect of Honey Bee (Apis mellifera) Supplementation and Efficiency of Other Pollinators. Biology, 14: 599. DOI: https://doi.org/10.3390/biology14060599
El-Sheikh, E.-S. A. & Galal, A. A. A. (2015). Toxic effects of sub-chronic exposure of male albino rats to emamectin benzoate and possible ameliorative role of Foeniculum vulgare essential oil. Environmental Toxicology and Pharmacology, 39: 1177-1188. DOI: https://doi.org/10.1016/j.etap.2015.04.008
Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., Aizen, M. A., Bommarco, R., Cunningham, S. A., Kremen, C., Carvalheiro, L. G., Harder, L. D., Afik, O., Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N. P., Dudenhöffer, J. H., Freitas, B. M., Ghazoul, J., Greenleaf, S., … Klein, A. M. (2013). Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance. Science, 339: 1608-1611. DOI: https://doi.org/10.1126/science.1230200
Heller, S., Joshi, N. K., Chen, J., Rajotte, E. G., Mullin, C. & Biddinger, D. J. (2020). Pollinator exposure to systemic insecticides and fungicides applied in the previous fall and pre-bloom period in apple orchards. Environmental Pollution, 265: 114589. DOI: https://doi.org/10.1016/j.envpol.2020.114589
Hesselbach, H., Seeger, J., Schilcher, F., Ankenbrand, M. & Scheiner, R. (2020). Chronic exposure to the pesticide flupyradifurone can lead to premature onset of foraging in honeybees Apis mellifera. Journal of Applied Ecology, 57: 609-618. DOI: https://doi.org/10.1111/1365-2664.13555
Hyne, R. V. & Maher, W. A. (2003). Invertebrate biomarkers: Links to toxicosis that predict population decline. Ecotoxicology and Environmental Safety, 54: 366-374. DOI: https://doi.org/10.1016/S0147-6513(02)00119-7
Johansen, C. A. & Mayer, D. F. (1990). Pollinator protection: A bee & pesticide handbook. Wicwas Press.
Johnson, R. M., Pollock, H. S. & Berenbaum, M. R. (2009). Synergistic Interactions Between In-Hive Miticides in Apis DOI: https://doi.org/10.1603/029.102.0202
mellifera. Journal of Economic Entomology, 102: 474-479.
Klein, A.-M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C. & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274: 303-313. DOI: https://doi.org/10.1098/rspb.2006.3721
Kueh Tai, F., Pattemore, D. E., Jochym, M., Beggs, J. R., Northcott, G. L. & Mortensen, A. N. (2022). Honey bee toxicological responses do not accurately predict environmental risk of imidacloprid to a solitary ground-nesting bee species. Science of The Total Environment, 839: 156398. DOI: https://doi.org/10.1016/j.scitotenv.2022.156398
Lehmann, D.M. & Camp, A.A. (2021). A systematic scoping review of the methodological approaches and effects of pesticide exposure on solitary bees. PLOS ONE, 16: e0251197. DOI: https://doi.org/10.1371/journal.pone.0251197
Leonard, R. J. & Harmon-Threatt, A. N. (2019). Methods for rearing ground-nesting bees under laboratory conditions. Apidologie, 50: 689-703. DOI: https://doi.org/10.1007/s13592-019-00679-8
Lundin, O., Rundlöf, M., Jonsson, M., Bommarco, R. & Williams, N.M. (2021). Integrated pest and pollinator management – expanding the concept. Frontiers in Ecology and the Environment, 19: 283-291. DOI: https://doi.org/10.1002/fee.2325
Mamood, A.N. & Waller, G.D. (1990). Recovery of learning responses by honeybees following a sublethal exposure to permethrin. Physiological Entomology, 15: 55-60. DOI: https://doi.org/10.1111/j.1365-3032.1990.tb00492.x
Manjon, C., Troczka, B. J., Zaworra, M., Beadle, K., Randall, E., Hertlein, G., Singh, K. S., Zimmer, C. T., Homem, R. A., Lueke, B., Reid, R., Kor, L., Kohler, M., Benting, J., Williamson, M. S., Davies, T. G. E., Field, L. M., Bass, C. & Nauen, R. (2018). Unravelling the Molecular Determinants of Bee Sensitivity to Neonicotinoid Insecticides. Current Biology, 28: 1137-1143.e5. DOI: https://doi.org/10.1016/j.cub.2018.02.045
Medrzycki, P., Sgolastra, F., Bortolotti, L., Bogo, G., Tosi, S., Padovani, E., Porrini, C. & Sabatini, A. G. (2010). Influence of brood rearing temperature on honey bee development and susceptibility to poisoning by pesticides. Journal of Apicultural Research, 49: 52-59. DOI: https://doi.org/10.3896/IBRA.1.49.1.07
Merle, I., Hipólito, J. & Requier, F. (2022). Towards integrated pest and pollinator management in tropical crops. Current Opinion in Insect Science, 50: 100866. DOI: https://doi.org/10.1016/j.cois.2021.12.006
Mode of Action | Insecticide Resistance Action Committee (IRAC). (2025, January 20). Insecticide Resistance Action Committee. https://irac-online.org/mode-of-action/
Nath, R., Singh, H. & Mukherjee, S. (2023). Insect pollinators decline: An emerging concern of Anthropocene epoch. Journal of Apicultural Research, 62: 23-38. DOI: https://doi.org/10.1080/00218839.2022.2088931
Nchang, E. C., Nkontcheu, D. B. K., Taboue, G. C. T., Bonwen, F. R. & Fokam, E. B. (2023). Pesticides drive patterns of insect visitors and pollination-related attributes of four crops in Buea, Southwest Cameroon. International Journal of Tropical Insect Science, 44: 117-128. DOI: https://doi.org/10.1007/s42690-023-01138-9
O’Reilly, A. D. & Stanley, D. A. (2023). Solitary bee behaviour and pollination service delivery is differentially impacted by neonicotinoid and pyrethroid insecticides. Science of The Total Environment, 894: 164399. DOI: https://doi.org/10.1016/j.scitotenv.2023.164399
Peterson, E. M., Green, F. B. & Smith, P. N. (2021). Toxic responses of blue orchard mason bees (Osmia lignaria) following contact exposure to neonicotinoids, macrocyclic lactones, and pyrethroids. Ecotoxicology and Environmental Safety, 208: 111681. DOI: https://doi.org/10.1016/j.ecoenv.2020.111681
Picard-Nizou, A. L., Pham-Delègue, M. H., Kerguelen, V., Douault, P., Marilleau, R., Olsen, L., Grison, R., Toppan, A. & Masson, C. (1995). Foraging behaviour of honey bees (Apis mellifera L.) on transgenic oilseed rape (Brassica napus L.var. Oleifera). Transgenic Research, 4: 270-276. DOI: https://doi.org/10.1007/BF01969121
Pontarp, M., Runemark, A., Friberg, M., Opedal, Ø. H., Persson, A. S., Wang, L. & Smith, H. G. (2024). Evolutionary plant-pollinator responses to anthropogenic land‐use change: Impacts on ecosystem services. Biological Reviews, 99: 372-389. DOI: https://doi.org/10.1111/brv.13026
Proesmans, W., Felten, E., Laurent, E., Albrecht, M., Cyrille, N., Labonté, A., Maurer, C., Paxton, R., Schweiger, O., Szentgyörgyi, H. & Vanbergen, A. J. (2024). Urbanisation and agricultural intensification modulate plant-pollinator network structure and robustness. Functional Ecology, 38: 628-641. DOI: https://doi.org/10.1111/1365-2435.14503
Qualls, W. A., Xue, R.-D. & Zhong, H. (2010). Impact of Bifenthrin on Honeybees and Culex quinquefasciatus. Journal of the American Mosquito Control Association, 26: 223-225. DOI: https://doi.org/10.2987/09-5956.1
Rauf, A., Saeed, S., Ali, M. & Nadeem Tahir, M. H. (2021). Comparative Efficiency of Native Insect Pollinators in Reproductive Performance of Medicago sativa L. in Pakistan. Insects, 12: 1029. DOI: https://doi.org/10.3390/insects12111029
Rieth, J. P. & Levin, M. D. (1988). The repellent effect of two pyrethroid insecticides on the honey bee. Physiological Entomology, 13: 213-218. DOI: https://doi.org/10.1111/j.1365-3032.1988.tb00925.x
Rondeau, S. & Raine, N. E. (2024). Single and combined exposure to ‘bee safe’ pesticides alter behaviour and offspring production in a ground-nesting solitary bee (Xenoglossa pruinosa). Proceedings of the Royal Society B: Biological Sciences, 291: 20232939. DOI: https://doi.org/10.1098/rspb.2023.2939
Sanchez-Bayo, F. & Goka, K. (2014). Pesticide Residues and Bees – A Risk Assessment. PLoS ONE, 9: e94482. DOI: https://doi.org/10.1371/journal.pone.0094482
Sgolastra, F., Hinarejos, S., Pitts-Singer, T. L., Boyle, N. K., Joseph, T., Lūckmann, J., Raine, N. E., Singh, R., Williams, N. M. & Bosch, J. (2019). Pesticide Exposure Assessment Paradigm for Solitary Bees. Environmental Entomology, 48: 22-35. DOI: https://doi.org/10.1093/ee/nvy105
Shi, X., Ma, C., De Kraker, J., Gong, S., Hodgson, J. A., Luo, S., Van Der Steen, J. J. M., Xiao, H., Wang, F., Tie, X., Chen, Z. & Zou, Y. (2024). Influence of agricultural intensification on pollinator pesticide exposure, food acquisition and diversity. Journal of Applied Ecology, 61: 1905-1917. DOI: https://doi.org/10.1111/1365-2664.14701
Sies, H. (1997). Oxidative stress: Oxidants and antioxidants. Experimental Physiology, 82: 291-295. DOI: https://doi.org/10.1113/expphysiol.1997.sp004024
Smart, L.E. & Stevenson, J.H. (1982). Laboratory Estimation of Toxicity of Pyrethroid Insecticides to Honeybees: Relevance to Hazard in the Field. Bee World, 63: 150-152. DOI: https://doi.org/10.1080/0005772X.1982.11097888
Sparks, T. C. (2025). Insecticide mixtures – Uses, benefits and considerations. Pest Management Science, 81: 1137-1144. DOI: https://doi.org/10.1002/ps.7980
Sponsler, D. B. & Johnson, R. M. (2016). Mechanistic modeling of pesticide exposure: The missing keystone of honey bee toxicology. Environmental Toxicology and Chemistry, 36: 871-881. DOI: https://doi.org/10.1002/etc.3661
Stanley, J., Chandrasekaran, S., Preetha, G., & Kuttalam, S. (2010). Toxicity of diafenthiuron to honey bees in laboratory, semi-field and field conditions: Toxicity of diafenthiuron to bees under different conditions. Pest Management Science, 66: 505–510. DOI: https://doi.org/10.1002/ps.1900
Stark, J. D., Jepson, P. C. & Mayer, D. F. (1995). Limitations to Use of Topical Toxicity Data for Predictions of Pesticide Side Effects in the Field. Journal of Economic Entomology, 88: 1081-1088. DOI: https://doi.org/10.1093/jee/88.5.1081
Tong, Z.-Y., Wu, L.-Y., Feng, H.-H., Zhang, M., Armbruster, W. S., Renner, S. S. & Huang, S.-Q. (2023). New calculations indicate that 90% of flowering plant species are animal-pollinated. National Science Review, 10: nwad219. DOI: https://doi.org/10.1093/nsr/nwad219
Uwingabire, Z. & Gallai, N. (2024). Impacts of degraded pollination ecosystem services on global food security and nutrition. Ecological Economics, 217: 108068. DOI: https://doi.org/10.1016/j.ecolecon.2023.108068
Vidau, C., Diogon, M., Aufauvre, J., Fontbonne, R., Viguès, B., Brunet, J.-L., Texier, C., Biron, D. G., Blot, N., El Alaoui, H., Belzunces, L. P. & Delbac, F. (2011). Exposure to Sublethal Doses of Fipronil and Thiacloprid Highly Increases Mortality of Honeybees Previously Infected by Nosema ceranae. PLoS ONE, 6: e21550. DOI: https://doi.org/10.1371/journal.pone.0021550
Wagan, S. A., Memon, Q. U. A., Tan, Y., Damalas, C. A., Memon, A., Sheikh, M. J. & Khushk, G. M. (2025). Farmers’ knowledge of pests and decision for pesticide selection in cotton: Impact on production efficiency levels in southern Pakistan. International Journal of Pest Management, 71: 343-352. DOI: https://doi.org/10.1080/09670874.2023.2209041
Wahl, O. & Ulm, K. (1983). Influence of pollen feeding and physiological condition on pesticide sensitivity of the honey bee Apis mellifera carnica. Oecologia, 59: 106-128. DOI: https://doi.org/10.1007/BF00388082
Williams, G.R., Alaux, C., Costa, C., Csáki, T., Doublet, V., Eisenhardt, D., Fries, I., Kuhn, R., McMahon, D.P., Medrzycki, P., Murray, T.E., Natsopoulou, M. E., Neumann, P., Oliver, R., Paxton, R.J., Pernal, S. F., Shutler, D., Tanner, G., Van Der Steen, J.J.M. & Brodschneider, R. (2013). Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. Journal of Apicultural Research, 52: 1-36. DOI: https://doi.org/10.3896/IBRA.1.52.1.04
Williams, G. R., Troxler, A., Retschnig, G., Roth, K., Yañez, O., Shutler, D., Neumann, P. & Gauthier, L. (2015). Neonicotinoid pesticides severely affect honey bee queens. Scientific Reports, 5: 14621. DOI: https://doi.org/10.1038/srep14621
Winston, M. L. (1991). The biology of the honey bee (1. Harvard Univ. Press paperback ed). Harvard University Press.
Zhang, Z., Huang, J., Yao, Y., Peters, G., Macdonald, B., La Rosa, A. D., Wang, Z. & Scherer, L. (2023). Environmental impacts of cotton and opportunities for improvement. Nature Reviews Earth & Environment, 4: 703-715. DOI: https://doi.org/10.1038/s43017-023-00476-z
Zhou, T., Zhou, W., Wang, Q., Dai, P.-L., Liu, F., Zhang, Y.-L. & Sun, J.-H. (2011). Effects of pyrethroids on neuronal excitability of adult honeybees Apis mellifera. Pesticide Biochemistry and Physiology, 100: 35-40. DOI: https://doi.org/10.1016/j.pestbp.2011.02.001
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2026 Fayyaz Hussain, Mudssar Ali, Fawad Zafar Ahmad Khan, Ahmad Ibrahim Jalali

This work is licensed under a Creative Commons Attribution 4.0 International License.
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).

eISSN 2447-8067









