Acute Toxicity of Selected Insecticides on Apis mellifera and Ceratina smaragdula: Laboratory and Field Assessments

Authors

  • Fayyaz Hussain Department of Entomology, Muhammad Nawaz Shareef University of Agriculture Multan, Multan, Pakistan
  • Mudssar Ali Department of entomology, Muhammad Nawaz Shareef University of Agriculture, Multan, Pakistan
  • Fawad Zafar Ahmad Khan Department of Entomology & Department of Outreach and Continuing Education, Muhammad Nawaz Shareef University of Agriculture Multan, Multan, Pakistan
  • Ahmad Ibrahim Jalali Department of Outreach and Continuing Education, Muhammad Nawaz Shareef University of Agriculture Multan, Multan, Pakistan

DOI:

https://doi.org/10.13102/sociobiology.v73i3.11980

Keywords:

honey bee, solitary bee, pesticides, IPPM

Abstract

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.

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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

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2026-08-06

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Hussain, F., Ali, M., Khan, F. Z. A., & Jalali, A. I. (2026). Acute Toxicity of Selected Insecticides on Apis mellifera and Ceratina smaragdula: Laboratory and Field Assessments. Sociobiology, 73(3), e11980. https://doi.org/10.13102/sociobiology.v73i3.11980

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Research Article - Bees