Fungicides, herbicides and bees: A systematic review of existing research and methods

Autoři: Merissa G. Cullen aff001;  Linzi J. Thompson aff002;  James. C. Carolan aff001;  Jane C. Stout aff004;  Dara A. Stanley aff002
Působiště autorů: Department of Biology, Maynooth University, Maynooth, Co. Kildare, Ireland aff001;  School of Agriculture and Food Science, University College Dublin, Belfield, Dublin, Ireland aff002;  Earth Institute, University College Dublin, Belfield, Dublin, Ireland aff003;  School of Natural Sciences, Trinity College Dublin, Dublin, Ireland aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


Bees and the pollination services they deliver are beneficial to both food crop production, and for reproduction of many wild plant species. Bee decline has stimulated widespread interest in assessing hazards and risks to bees from the environment in which they live. While there is increasing knowledge on how the use of broad-spectrum insecticides in agricultural systems may impact bees, little is known about effects of other pesticides (or plant protection products; PPPs) such as herbicides and fungicides, which are used more widely than insecticides at a global scale. We adopted a systematic approach to review existing research on the potential impacts of fungicides and herbicides on bees, with the aim of identifying research approaches and determining knowledge gaps. While acknowledging that herbicide use can affect forage availability for bees, this review focussed on the potential impacts these compounds could have directly on bees themselves. We found that most studies have been carried out in Europe and the USA, and investigated effects on honeybees. Furthermore, certain effects, such as those on mortality, are well represented in the literature in comparison to others, such as sub-lethal effects. More studies have been carried out in the lab than in the field, and the impacts of oral exposure to herbicides and fungicides have been investigated more frequently than contact exposure. We suggest a number of areas for further research to improve the knowledge base on potential effects. This will allow better assessment of risks to bees from herbicides and fungicides, which is important to inform future management decisions around the sustainable use of PPPs.

Klíčová slova:

Bees – Bumblebees – Fungicides – Herbicides – Honey bees – Insecticides – Pesticides – Pollen


1. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, et al. Importance of pollinators in changing landscapes for world crops. Proc B. 2007;274(1608):303–13.

2. Ollerton J, Winfree R, Tarrant S. How many flowering plants are pollinated by animals? Oikos. 2011;120(3):321–6.

3. Gallai N, Salles JM, Settele J, Vaissiere BE. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics. 2009;68(3):810–21.

4. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemuller R, Edwards M, Peeters T, et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science. 2006;313(5785):351–4. doi: 10.1126/science.1127863 16857940

5. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, et al. Patterns of widespread decline in North American bumble bees. PNAS. 2011;108(2):662–7. doi: 10.1073/pnas.1014743108 21199943

6. Ollerton J, Erenler H, Edwards M, Crockett R. Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science. 2014;346(6215):1360–2. doi: 10.1126/science.1257259 25504719

7. IPBES. Summary for policymakers of the assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. Bonn, Germany: Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, 2016.

8. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution. 2010;25(6):345–53.

9. Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, et al. Safeguarding pollinators and their values to human well-being. Nature. 2016;540:220–9. doi: 10.1038/nature20588 27894123

10. 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).

11. Cooper J, Dobson H. The benefits of pesticides to mankind and the environment. Crop Protection. 2007;26(9):1337–48.

12. Carvalho FP. Pesticides, environment, and food safety. Food and Energy Security. 2017;6(2):48–60.

13. Bass C, Puinean AM, Zimmer CT, Denholm I, Field LM, Foster SP, et al. The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochemistry and Molecular Biology. 2014;51:41–51. doi: 10.1016/j.ibmb.2014.05.003 24855024

14. Van Bruggen AHC, He MM, Shin K, Mai V, Jeong KC, Finckh MR, et al. Environmental and health effects of the herbicide glyphosate. Science of The Total Environment. 2018;616–617:255–68.

15. Silva V, Mol HGJ, Zomer P, Tienstra M, Ritsema CJ, Geissen V. Pesticide residues in European agricultural soils–A hidden reality unfolded. Science of The Total Environment. 2019;653:1532–45. doi: 10.1016/j.scitotenv.2018.10.441 30759587

16. 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:e0136928. doi: 10.1371/journal.pone.0136928 26313444

17. Wood TJ, Goulson D. The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ Sci Pollut Res. 2017;24(21):17285–325.

18. Godfray HCJ, Blacquière T, Field LM, Hails RS, Petrokofsky G, Potts SG, et al. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B- Biological Sciences. 2014;281(20140558):20140558.

19. Godfray HCJ, Blacquière T, Field LM, Hails RS, Potts SG, Raine NE, et al. A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B- Biological Sciences. 2015;282(1818):20151821. doi: 10.1098/rspb.2015.1821 26511042

20. Blacquiere T, Smagghe G, van Gestel CAM, Mommaerts V. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology. 2012;21(4):973–92. doi: 10.1007/s10646-012-0863-x 22350105

21. Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, et al. Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res. 2015;22(1):68–102.

22. Pisa L, Goulson D, Yang EC, Gibbons D, Sanchez-Bayo F, Mitchell E, et al. An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems. Environmental science and pollution research international. 2017:1–49.

23. EUROSTAT. Agri-environmental indicator—consumption of pesticides 2018 [11/2/2019]. Available from:

24. Jess S, Matthews DI, Murchie AK, Lavery MK. Pesticide Use in Northern Ireland's Arable Crops from 1992–2016 and Implications for Future Policy Development. Agriculture-Basel. 2018;8(8).

25. Pesticides Industry Sales and Usage [Internet]. United States Environmental Protection Agency; 2017. Available from:

26. Heap I, Duke SO. Overview of glyphosate-resistant weeds worldwide. Pest Management Science. 2018;74(5):1040–9. doi: 10.1002/ps.4760 29024306

27. Mortensen DA, Egan JF, Maxwell BD, Ryan MR, Smith RG. Navigating a critical juncture for sustainable weed management. BioScience. 2012;62(1):75–84.

28. Rinsky JL, Hopenhayn C, Golla V, Browning S, Bush HM. Atrazine exposure in public drinking water and preterm birth. Public Health Rep. 2012;127(1):72–80. doi: 10.1177/003335491212700108 22298924

29. Silva V, Montanarella L, Jones A, Fernández-Ugalde O, Mol HGJ, Ritsema CJ, et al. Distribution of glyphosate and aminomethylphosphonic acid (AMPA) in agricultural topsoils of the European Union. Science of The Total Environment. 2018;621:1352–9. doi: 10.1016/j.scitotenv.2017.10.093 29042088

30. Casado J, Brigden K, Santillo D, Johnston P. Screening of pesticides and veterinary drugs in small streams in the European Union by liquid chromatography high resolution mass spectrometry. Science of The Total Environment. 2019;670:1204–25. doi: 10.1016/j.scitotenv.2019.03.207 31018436

31. Chowdhary A, Kathuria S, Xu J, Meis JF. Emergence of azole-resistant Aspergillus fumigatus strains due to agricultural azole use creates an increasing threat to human health. PLOS Pathogens. 2013;9(10):e1003633. doi: 10.1371/journal.ppat.1003633 24204249

32. Zhang L, Rana I, Shaffer RM, Taioli E, Sheppard L. Exposure to glyphosate-based herbicides and risk for Non-Hodgkin Lymphoma: A meta-analysis and supporting evidence. Mutation Research/Reviews in Mutation Research. 2019;781:186–206.

33. Mengoni Goñalons C, Farina WM. Impaired associative learning after chronic exposure to pesticides in young adult honey bees. The Journal of Experimental Biology. 2018;221(7):jeb176644.

34. Dai P, Yan Z, Ma S, Yang Y, Wang Q, Hou C, et al. The herbicide glyphosate negatively affects midgut bacterial communities and survival of honey bee during larvae reared in vitro. J Agric Food Chem. 2018;66(29):7786–93. doi: 10.1021/acs.jafc.8b02212 29992812

35. Balbuena MS, Tison L, Hahn ML, Greggers U, Menzel R, Farina WM. Effects of sublethal doses of glyphosate on honeybee navigation. J Exp Biol. 2015;218(Pt 17):2799–805. doi: 10.1242/jeb.117291 26333931

36. Liao L-H, Wu W-Y, Berenbaum MR. Behavioral responses of honey bees (Apis mellifera) to natural and synthetic xenobiotics in food. Scientific Reports. 2017;7(1):15924. doi: 10.1038/s41598-017-15066-5 29162843

37. Mao W, Schuler MA, Berenbaum MR. Disruption of quercetin metabolism by fungicide affects energy production in honey bees (Apis mellifera). Proc Natl Acad Sci USA. 2017;114(10):2538–43. doi: 10.1073/pnas.1614864114 28193870

38. Cizelj I, Glavan G, Božič J, Oven I, Mrak V, Narat M. Prochloraz and coumaphos induce different gene expression patterns in three developmental stages of the Carniolan honey bee (Apis mellifera carnica Pollmann). Pesticide Biochemistry and Physiology. 2016;128:68–75. doi: 10.1016/j.pestbp.2015.09.015 26969442

39. Lewis KA, Tzilivakis J, Warner DJ, Green A. An international database for pesticide risk assessments and management. Human and Ecological Risk Assessment: An International Journal. 2016;22(4):1050–64.

40. Desneux N, Decourtye A, Delpuech J-M. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology. 2007;52:81–106. doi: 10.1146/annurev.ento.52.110405.091440 16842032

41. Schreinemachers P, Tipraqsa P. Agricultural pesticides and land use intensification in high, middle and low income countries. Food Policy. 2012;37(6):616–26.

42. Kleijn D, Winfree R, Bartomeus I, Carvalheiro LG, Henry M, Isaacs R, et al. Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nature Communications. 2015;6:7414 doi: 10.1038/ncomms8414 26079893

43. Michener CD. The Bees of the World: John Hopkins University Press; 2007.

44. Rundlöf M, Andersson GKS, Bommarco R, Fries I, Hederstrom V, Herbertsson L, et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature. 2015;521(7550):77–80. doi: 10.1038/nature14420 25901681

45. 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):1393–5. doi: 10.1126/science.aaa1190 28663502

46. Arena M, Sgolastra F. A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology. 2014;23(3):324–34. doi: 10.1007/s10646-014-1190-1 24435220

47. Piiroinen S, Goulson D. Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees. Proceedings of the Royal Society B- Biological Sciences. 2016;283(1828):20160246.

48. Cresswell JE, Page CJ, Uygun MB, Holmbergh M, Li Y, Wheeler JG, et al. Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology. 2012;115(6):365–71. doi: 10.1016/j.zool.2012.05.003 23044068

49. Boyle NK, Pitts-Singer TL, Abbott J, Alix A, Cox-Foster DL, Hinarejos S, et al. Workshop on Pesticide Exposure Assessment Paradigm for Non-Apis Bees: Foundation and Summaries. Environmental Entomology. 2018;48(1):4–11.

50. Sgolastra F, Hinarejos S, Pitts-Singer TL, Boyle NK, Joseph T, Lūckmann J, et al. Pesticide exposure assessment paradigm for solitary bees. Environmental Entomology. 2018;48(1):22–35.

51. David A, Botías C, Abdul-Sada A, Nicholls E, Rotheray EL, Hill EM, et al. Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environment International. 2016;88:169–78. doi: 10.1016/j.envint.2015.12.011 26760714

52. Böhme F, Bischoff G, Zebitz CPW, Rosenkranz P, Wallner K. Pesticide residue survey of pollen loads collected by honeybees (Apis mellifera) in daily intervals at three agricultural sites in South Germany. PLOS ONE. 2018;13(7):e0199995. doi: 10.1371/journal.pone.0199995 29979756

53. Power EF, Stout JC. Organic dairy farming: impacts on insect-flower interaction networks and pollination. Journal of Applied Ecology. 2011;48(3):561–9.

54. Gabriel D, Tscharntke T. Insect pollinated plants benefit from organic farming. Agriculture, Ecosystems & Environment. 2007;118(1–4):43–8.

55. Motta EVS, Raymann K, Moran NA. Glyphosate perturbs the gut microbiota of honey bees. Proceedings of the National Academy of Sciences. 2018;115(41):10305–10.

56. Chan DSW, Prosser RS, Rodríguez-Gil JL, Raine NE. Assessment of risk to hoary squash bees (Peponapis pruinosa) and other ground-nesting bees from systemic insecticides in agricultural soil. Scientific Reports. 2019;9(1):11870. doi: 10.1038/s41598-019-47805-1 31413274

57. Cresswell J. A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology. 2011;20(1):149–57. doi: 10.1007/s10646-010-0566-0 21080222

58. 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):2812–21. doi: 10.1111/1365-2664.13193 30449899

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden