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Journals / Uludağ Arıcılık Dergisi / 2026 / Volume: 26

Pesticide effects on bee behavior and cognition: a bibliometric analysis of global research (2000–2025)

İsmail Yaşhan Buluş(MUŞ ALPARSLAN ÜNİVERSİTESİ)0000-0003-4418-588X
Pages
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Publication Date
2026-10-19
🏛️Bibliographic metadata and full text access for this article are provided via DergiPark.
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AI Summary & Key Takeaways

AI Insight
⚡ TL;DR(Too Long; Didn't Read)

Results showed a marked increase in research output after 2015, with peak productivity in 2023.

📌 3 Key Takeaways

🎯
Objective & Hypothesis:Bees are essential for ecosystem stability and global food security, yet their populations are declining worldwide, largely due to agrochemical exposure.
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Key Findings & Data:This study presents a bibliometric analysis of global research on the impacts of pesticides on bee behavior and cognition, based on 1,418 publications indexed in the Web of Science (2000–2025).
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Conclusion & Impact:Results showed a marked increase in research output after 2015, with peak productivity in 2023.
🔬Design:Research Article
📍Scope:2000–2025 Verileri
⚙️Variables:Bees · Behavior · Bibliometrics

Abstract

Bees are essential for ecosystem stability and global food security, yet their populations are declining worldwide, largely due to agrochemical exposure. Traditional pesticide risk assessments have focused on acute mortality, whereas recent ecotoxicological research increasingly emphasizes sublethal behavioral and cognitive effects. This study presents a bibliometric analysis of global research on the impacts of pesticides on bee behavior and cognition, based on 1,418 publications indexed in the Web of Science (2000–2025). Data were analyzed with the Bibliometrix R package and VOSviewer to identify publication trends, collaboration networks, and thematic evolution. Results showed a marked increase in research output after 2015, with peak productivity in 2023. The field is led by international collaborations centered in the United States, China, and Western Europe, with *Apidologie* serving as a key publication outlet. Thematic analyses revealed three major shifts: from mortality-based assessments to behavioral and cognitive endpoints such as learning, memory, and navigation; from traditional pesticides to newer compounds including flupyradifurone, sulfoxaflor, and thiacloprid; and from single-stressor approaches to multi-stressor frameworks integrating pesticide exposure with climate change, nutritional stress, and gut microbiota disruption. These findings highlight the need for regulatory frameworks that incorporate standardized behavioral, cognitive, and multi-stressor assessments to protect pollinator biodiversity and ecosystem services.

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Cite This Article

Buluş, İ. Y. (2026). Pesticide effects on bee behavior and cognition: a bibliometric analysis of global research (2000–2025). Uludağ Arıcılık Dergisi, Volume: 26. https://doi.org/10.31467/uluaricilik.1997375

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References (69)

  1. Abbo PM, Kawasaki JK, Hamilton M, Cook S C, DeGrandi‐Hoffman G, Li WF, et al. Effects of Imidacloprid and Varroa destructor on survival and health of European honey bees, Apis mellifera. Insect Science 2017;24(3):467–477. https://doi.org/10.1111/1744-7917.12335
  2. Abramson CI, Aquino IS, Ramalho FS, Price JM. The effect of insecticides on learning in the Africanized honey hee (Apis mellifera L.). Archives of Environmental Contamination and Toxicology 1999;37(4):529–535. https://doi. org/10.1007/s002449900548
  3. Al Naggar Y, Estrella-Maldonado H, Paxton RJ, Solís T, Quezada-Euán JJG. The insecticide imidacloprid decreases Nannotrigona stingless bee survival and food consumption and modulates the expression of detoxification and immune-related genes. Insects 2022;13(11):972. https://doi.org/ 10.3390/insects13110972
  4. Albacete S, Sancho G, Azpiazu C, Rodrigo A, Molowny‐Horas R, Sgolastra F, et al. Bees exposed to climate change are more sensitive to pesticides. Global Change Biology 2023;29(22):6248–6260. https://doi.org/10. 1111/gcb.16928
  5. Aria M, Cuccurullo C. bibliometrix: An R-tool for comprehensive science mapping analysis. Journal of Informetrics 2017;11(4):959–975. https://doi.org/10.1016/j.joi.2017.08.007
  6. Ayers GS, Wroblewska A, Hoopingarner RA. Perennial diversionary planting designed to reduce pesticide mortality of honey bees in apple orchards. American Bee Journal 1991;131(4), 247-252.
  7. Balbuena MS, Tison L, Hahn ML, Greggers U, Menzel R, Farina WM. Effects of sublethal doses of glyphosate on honeybee navigation. The Journal of Experimental Biology 2015;218(17):2799–2805. https://doi.org/ 10.1242/jeb.117291
  8. Bekić B, Jeločnik M, Subić J. Honey bee colony collapse disorder (Apis mellifera L.)-Possible causes. Scientific Papers Series Management, Economic Engineering in Agriculture and Rural Development 2014;14(2):13–18.
  9. Bird G, Wilson AE, Williams GR, Hardy NB. Parasites and pesticides act antagonistically on honey bee health. Journal of Applied Ecology 2021;58(5):997–1005. https:// doi.org/10.1111/1365-2664.13811
  10. Boff S, Scheiner R, Raizer J, Lupi D. Survival rate and changes in foraging performances of solitary bees exposed to a novel insecticide. Ecotoxicology and Environmental Safety 2021;211:111869. https://doi.org/10.1016/ j.ecoenv.2020.111869
  11. Botías C, Jones JC, Pamminger T, Bartomeus I, Hughes WO H, Goulson D. Multiple stressors interact to impair the performance of bumblebee Bombus terrestris colonies. Journal of Animal Ecology 2021;90(2):415–431. https://doi.org/10.1111/1365-2656.13375
  12. Cabirol A, Haase A. The neurophysiological bases of the impact of neonicotinoid pesticides on the behaviour of honeybees. Insects 2019;10(10):344. https://doi.org/10.3390/ insects10100344
  13. Capela N, Xu M, Simões S, Azevedo-Pereira HM, Peters J, Sousa JP. Exposure and risk assessment of acetamiprid in honey bee colonies under a real exposure scenario in Eucalyptus sp. Landscapes. Science of the Total Environment 2022;840:156485. https://doi.org/10.1016/j.scitotenv.2022.156485
  14. Cappa F, Baracchi D. Bioinsecticides on honey bees: Exposure, sublethal effects, and risk assessment paradigms. Current Opinion in Environmental Science & Health 2024;41: 100569. https://doi.org/10.1016/j.coesh. 2024.100569
  15. Colin T, Meikle WG, Wu X, Barron AB. Traces of a neonicotinoid induce precocious foraging and reduce foraging performance in honey bees. Environmental Science & Technology 2019;53(14):8252–8261. https://doi.org/ 10.1021/acs.est.9b02452
  16. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, et al. A Metagenomic Survey of Microbes in Honey Bee Colony Collapse Disorder. Science 2007;318(5848):283–287. https://doi.org/ 10.1126/science.1146498
  17. Demirozer O, Uzun A, Yanik G, Bulus IY, Gosterit A. Investigation of the efficacy of some biopesticides by food exposure on Bombus terrestris L. (Hymenoptera: Apidae). Journal of Apicultural Research 2023;62(5):1153–1157. https://doi.org/10.1080/00218839. 2022.2054538
  18. Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, Nazzi F, et al. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences 2013;110(46):18466–18471. https://doi.org/10.1073/pnas. 1314923110
  19. Dirilgen T, Herbertsson L, O’reilly AD, Mahon N, Stanley DA. Moving past neonicotinoids and honeybees: A systematic review of existing research on other insecticides and bees. Environmental Research 2023;235:116612. https://doi.org/10.1016/j.envres.2023.116612
  20. Doublet V, Labarussias M, De Miranda JR, Moritz RFA, Paxton RJ. Bees under stress: Sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environmental Microbiology 2015;17(4):969–983. https:// doi.org/10.1111/1462-2920.12426
  21. Eiri DM, Nieh JC. A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. Journal of Experimental Biology 2012;215(12):2022–2029. https://doi.org/ 10.1242/jeb.068718
  22. Ellis JD, Evans JD, Pettis J. Colony losses, managed colony population decline, and Colony Collapse Disorder in the United States. Journal of Apicultural Research 2010;49(1):134–136. https://doi.org/10.3896/ IBRA.1.49.1.30
  23. European Commission. Bee Health: EU takes additional measures on pesticides to better protect Europe’s bees. European Food Safety Authority 2013, https://ec.europa.eu/ commission/presscorner/detail/en/ip_13_708 (retrieved by: 17.05.2026).
  24. Ferreira PA, Boscolo D, Carvalheiro LG, Biesmeijer JC, Rocha PLB, Viana BF. Responses of bees to habitat loss in fragmented landscapes of Brazilian Atlantic Rainforest. Landscape Ecology 2015;30(10):2067–2078. https://doi. org/10.1007/s10980-015-0231-3
  25. Fischer J, Müller T, Spatz AK, Greggers U, Grünewald B, Menzel R. Neonicotinoids interfere with specific components of navigation in honeybees. PloS One 2014;9(3):e91364. https://doi.org/10.1371/ journal.pone.0091364
  26. Free JB, Ferguson AW. Foraging of bees on oil-seed rape (Brassica napus L.) in relation to the stage of flowering of the crop and pest control. The Journal of Agricultural Science 1980;94(1):151–154. https://doi.org/10.1017/ S0021859600028008
  27. Ghisbain G, Thiery W, Massonnet F, Erazo D, Rasmont P, Michez D, et al. Projected decline in European bumblebee populations in the twenty-first century. Nature 2024;628(8007): 337–341. https://doi.org/ 10.1038/s41586-023-06471-0
  28. Gill RJ, Raine NE. Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Functional Ecology 2014;28(6):1459–1471. https://doi. org/10.1111/1365-2435.12292
  29. Goulson D, Nicholls E, Botías C, Rotheray EL. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 2015;347(6229):1255957. https:// doi.org/10.1126/science.1255957
  30. Guez D. A common pesticide decreases foraging success and survival in honey bees: Questioning the ecological relevance. Frontiers in Physiology 2013;4:37. https://doi.org/10.3389/fphys.2013.00037
  31. Guo Y, Diao QY, Dai PL, Wang Q, Hou CS, Liu YJ, et al. The effects of exposure to flupyradifurone on survival, development, and foraging activity of honey bees (Apis mellifera L.) under field conditions. Insects 2021;12(4):357. https://doi.org/10.3390/ insects12040357
  32. Hagler JR, Waller GD, Lewis BE. Mortality of Honeybees (Hymenoptera: Apidae) Exposed to Permethrin and Combinations of Permethrin with Piperonyl Butoxide. Journal of Apicultural Research 1989;28(4):208–211. https://doi.org/10.1080/00218839.1989.11101186
  33. Harwood GP, Dolezal AG. Pesticide–virus interactions in honey bees: Challenges and opportunities for understanding drivers of bee declines. Viruses 2020;12(5):566. https:// doi.org/10.3390/v12050566
  34. Henry M, Béguin M, Requier F, Rollin O, Odoux JF, Aupinel P, et al. A common pesticide decreases foraging success and survival in honey bees. Science 2012;336(6079):348–350. https://doi.org/10.1126/science.1215039
  35. Iwasaki JM, Hogendoorn K. Non-insecticide pesticide impacts on bees: A review of methods and reported outcomes. Agriculture, Ecosystems & Environment 2021;314: 107423. https://doi.org/10.1016/j.agee.2021. 107423
  36. Janousek WM, Douglas MR, Cannings S, Clément MA, Delphia CM, Everett JG, et al. Recent and future declines of a historically widespread pollinator linked to climate, land cover, and pesticides. Proceedings of the National Academy of Sciences 2023;120(5): e2211223120. https://doi.org/10.1073/pnas. 2211223120
  37. Jie C, Zhang H, Zhou Z, Miao Z, Han B, Guo B, et al. Flupyradifurone Exhibits Greater Toxicity to the Asian Bumblebee Bombus lantschouensis Compared to the European Bombus terrestris. Insects 2025;16(5):455. https://doi.org/ 10.3390/insects16050455
  38. Kenna D, Cooley H, Pretelli I, Ramos Rodrigues A, Gill SD, Gill RJ. Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees. Ecology and Evolution 2019;9(10):5637–5650. https://doi.org/ 10.1002/ece3.5143
  39. Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, et al. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 2007;274(1608):303–313. https://doi.org/ 10.1098/rspb.2006.3721
  40. Kline O, Joshi NK. Mitigating the effects of habitat loss on solitary bees in agricultural ecosystems. Agriculture 2020;10(4):115. https://doi.org/10.3390/agriculture10040115
  41. Lundin O, Rundlöf M, Smith HG, Fries I, Bommarco R. Neonicotinoid insecticides and their impacts on bees: A systematic review of research approaches and identification of knowledge gaps. PLoS One 2015;10(8):e0136928. https://doi.org/ 10.1371/journal.pone.0136928
  42. MacKenzie KE, Winston ML. The effects of sublethal exposure to diazinon, carbaryl and resmethrin on longevity and foraging in Apis mellifera L. Apidologie 1989;20(1):29–40. https://doi.org/ 10.1051/apido:19890104
  43. Margaoan R, Papa G, Nicolescu A, Cornea-Cipcigan M, Kösoğlu M, Topal E, et al. Environmental pollution effect on honey bees and their derived products: A comprehensive analysis. Environmental Science and Pollution Research 2024;32(16):10370–10391. https://doi.org/10.1007/s11356-024-33754-4
  44. Mengoni Goñalons C, Farina WM. Impaired associative learning after chronic exposure to pesticides in young adult honey bees. Journal of Experimental Biology 2018;221(7): jeb176644. https://doi.org/10.1242/jeb. 176644
  45. Michener CD. The bees of the world. JHU Press, Baltimore, Maryland, USA, 2007, p.1-953.
  46. Nemésio A, Silva DP, Nabout JC, Varela S. Effects of climate change and habitat loss on a forest‐dependent bee species in a tropical fragmented landscape. Insect Conservation and Diversity 2016;9(2):149–160. https:// doi.org/10.1111/icad.12154
  47. Nowakowski J, Morse RA. The behavior of honey bees in sweet corn fields in New York State. American Bee Journal 1982;122(1), 13-16.
  48. Paoli M, Giurfa M. Pesticides and pollinator brain: How do neonicotinoids affect the central nervous system of bees? European Journal of Neuroscience 2024;60(8):5927–5948. https://doi.org/10.1111/ejn.16536
  49. Pereira NC, Diniz TO, Takasusuki M. Sublethal effects of neonicotinoids in bees: A review. Scientific Electronic Archives 2020;13(7):142–152. http://dx.doi.org/10. 36560/13720201120
  50. Pike KS, Mayer DF, Glazer M, Kious C. Effects of permethrin on mortality and foraging behavior of honey bees in sweet corn. Environmental Entomology 1982;11(4):951–953. https://doi. org/10.1093/ee/11.4.951
  51. Rundlöf M, Andersson GK, Bommarco R, Fries I, Hederström V, Herbertsson L, et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 2015;521(7550):77–80. https://doi.org/10. 1038/nature14420
  52. Serrão JE, Plata-Rueda A, Martínez LC, Zanuncio JC. Side-effects of pesticides on non-target insects in agriculture: A mini-review. The Science of Nature 2022;109(2):17. https://doi.org/10.1007/s00114-022-01788-8
  53. Shi J, Wang X, Luo Y. Honey bees prefer moderate sublethal concentrations of acetamiprid and experience increased mortality. Pesticide Biochemistry and Physiology 2025;208: 106320. https://doi.org/10.1016/j.pestbp. 2024.106320
  54. Siviter H, Bailes EJ, Martin CD, Oliver TR, Koricheva J, Leadbeater E, et al. Agrochemicals interact synergistically to increase bee mortality. Nature 2021;596(7872):389–392. https:// doi.org/10.1038/s41586-021-03787-7
  55. Siviter H, Koricheva J, Brown MJF, Leadbeater E. Quantifying the impact of pesticides on learning and memory in bees. Journal of Applied Ecology 2018;55(6):2812–2821. https://doi.org/10.1111/1365-2664.13193
  56. Soroye P, Newbold T, Kerr J. Climate change contributes to widespread declines among bumble bees across continents. Science 2020;367(6478):685–688. https://doi.org/ 10.1126/science.aax8591
  57. Stanley DA, Garratt MP, Wickens JB, Wickens VJ, Potts SG, Raine NE. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 2015;528(7583):548–550. https://doi.org/ 10.1038/nature16167
  58. Stanley DA, Smith KE, Raine NE. Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide. Scientific Reports 2015;5(1):16508. https:// doi.org/10.1038/srep16508
  59. Stuligross C, Williams NM. Pesticide and resource stressors additively impair wild bee reproduction. Proceedings of the Royal Society B: Biological Sciences 2020;287(1935):20201390. https://doi.org/ 10.1098/rspb.2020.1390
  60. Tan K, Wang C, Dong S, Li X, Nieh JC. The pesticide flupyradifurone impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Scientific Reports 2017;7(1):17772. https://doi.org/10.1038/ s41598-017-18060-z
  61. Tosi S, Burgio G, Nieh JC. A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Scientific Reports 2017;7(1):1201. https://doi.org/10.1038/ s41598-017-01361-8
  62. Tosi S, Nieh JC, Brandt A, Colli M, Fourrier J, Giffard H, et al. Long-term field-realistic exposure to a next-generation pesticide, flupyradifurone, impairs honey bee behaviour and survival. Communications Biology 2021;4(1):805. https://doi.org/10.1038/s41598-017-01361-8
  63. Van Eck N, Waltman L. Software survey: VOSviewer, a computer program for bibliometric mapping. Scientometrics 2010;84(2):523–538. https://doi.org/10.1007/ s11192-009-0146-3
  64. VanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, et al. Colony collapse disorder: A descriptive study. PloS One 2009;4(8):e6481. https://doi.org/ 10.1371/journal.pone.0006481
  65. Wan NF, Fu L, Dainese M, Kiær LP, Hu YQ, Xin F, et al. Pesticides have negative effects on non-target organisms. Nature Communications 2025;16(1):1360. https://doi.org/10.1038/ s41467-025-56732-x
  66. Whitehorn PR, Wallace C, Vallejo-Marín M. Neonicotinoid pesticide limits improvement in buzz pollination by bumblebees. Scientific Reports 2017;7(1):15562. https://doi.org/ 10.1038/s41598-017-14660-x
  67. Woodcock BA, Bullock JM, Shore RF, Heard MS, Pereira MG, Redhead J, et al. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 2017;356(6345):1393–1395. https://doi.org/ 10.1126/science.aaa1190
  68. Yang EC, Chuang YC, Chen YL, Chang LH. Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology 2008;101(6):1743–1748. https://doi.org/10.1603/0022-0493-101.6.1743
  69. Zhang ZY, Li Z, Huang Q, Yan WY, Zhang LZ, Zeng ZJ. Honeybees (Apis mellifera) modulate dance communication in response to pollution by imidacloprid. Journal of Asia-Pacific Entomology 2020;23(2):477–482. https://doi. org/10.1016/j.aspen.2020.03.011