Plant Soil Environ., 2023, 69(5):195-201 | DOI: 10.17221/86/2023-PSE

Effect of glyphosate on the foraging activity of European honey bees (Apis mellifera L.)Review

Aneta Bok¹ová1, Jan Kazda1, Jan Barto¹ka2, Martin Kamler3
1 Department of Plant Protection, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czech Republic
2 Department of Systems Engineering, Faculty of Economics and Management, Czech University of Life Sciences Prague, Prague, Czech Republic
3 Department of Research, Bee Research Institute, Dol, Czech Republic

Glyphosate is a widely used agrochemical. Nevertheless, only a few studies have investigated its effect on bees, specifically its influence on their foraging activity. This article provides a summary of the prominent research results on this issue, published in journals in the field of experimental biology. The effect of commonly used concentrations of glyphosate on honey bee navigation has been evaluated in several studies, as well as concentrations that are reportedly sublethal. Exposure to this herbicide increases the flight time back to the hive and affects the flight trajectories of these bees. These results imply that glyphosate at certain concentrations reduces their sensitivity to nectar rewards in associative memories. The contact of bees with non-lethal concentrations of glyphosate results in sublethal effects that affect foraging. In the future, the behaviour of glyphosate and its effect on bees in their natural environment need to be explored.

Keywords: plant protection; pollinator; bee memory; bee orientation; sugar syrup

Received: February 27, 2023; Revised: April 4, 2023; Accepted: April 12, 2023; Prepublished online: May 5, 2023; Published: May 31, 2023  Show citation

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Bok¹ová A, Kazda J, Barto¹ka J, Kamler M. Effect of glyphosate on the foraging activity of European honey bees (Apis mellifera L.). Plant Soil Environ. 2023;69(5):195-201. doi: 10.17221/86/2023-PSE.
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References

  1. Abraham J., Benhotons G.S., Krampah I., Tagba J., Amissah C., Abraham J.D. (2018): Commercially formulated glyphosate can kill non-target pollinator bees under laboratory conditions. Entomologia Experimentalis et Applicata, 166: 695-702. Go to original source...
  2. Aizen M.A., Garibaldi L.A., Cunningham S.A., Klein A.M. (2008): Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Current Biology, 18: 1572-1575. Go to original source... Go to PubMed...
  3. Alonso L.L., Ronco A.E., Marino D.J. (2014): Glyphosate and atrazine levels in rainwater from the Pampea region. In: Proceedings of the V Congreso Argentino SETAC, Neuqu én, Argentina, 40.
  4. Atanasov A.Z., Georgiev S.G., Vulkov L.G. (2021): Reconstruction analysis of honeybee colony collapse disorder modelling. Optimisation and Engineering, 22: 2481-2503. Go to original source...
  5. Balbuena M.S., Tison L., Hahn M., Greggers U., Menzel R., Farina W.M. (2015): Effects of sublethal doses of glyphosate on honeybee navigation. Journal of Experimental Biology, 218: 2799-2805. Go to original source... Go to PubMed...
  6. Belsky J., Joshi N.K. (2020): Effects of fungicide and herbicide chemical exposure on Apis and non-Apis bees in the agricultural landscape. Frontiers in Environmental Science, 8: 00081. Go to original source...
  7. Blot N., Veillat L., Rouzé R., Delatte H. (2019): Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota. PLOS One, 14: e0215466. Go to original source... Go to PubMed...
  8. Bommuraj V., Chen Y., Birenboim M., Barel S., Shimshoni J.A. (2021): Concentration- and time-dependent toxicity of commonly encountered pesticides and pesticide mixtures to honeybees (Apis mellifera L.). Chemosphere, 266: 128974. Go to original source... Go to PubMed...
  9. Brankov M., Simiæ M., Dragicevic V. (2021): The influence of maize - winter wheat rotation and pre-emergence herbicides on weeds and maize productivity. Crop Protection, 143: 105558. Go to original source...
  10. Chang F.C., Simcik M.F., Capel P.D. (2011): Occurrence and the fate of the herbicide glyphosate and its degradate aminomethylphosphonic acid in the atmosphere. Environmental Toxicology and Chemistry, 30: 548-555. Go to original source... Go to PubMed...
  11. Dai P., Yan Z., Ma S., Yang Y., Wang Q., Hou C., Wu Y., Liu Y., Diao Q. (2018): The herbicide glyphosate negatively affects midgut bacterial communities and survival of honey bee during larvae reared in vitro. Journal of Agricultural and Food Chemistry, 66: 7786-7793. Go to original source... Go to PubMed...
  12. De Souza A.P.F., Rodrigues N.R., Reyes F.G.R. (2021): Glyphosate and aminomethylphosphonic acid (AMPA) residues in Brazilian honey. Food Additives and Contaminants, Part B, Surveillance, 14: 40-47. Go to original source... Go to PubMed...
  13. De Stefano L.A., Stepanov I.I., Abramson C.I. (2014): The first order transfer function in the analysis of agrochemical data in honey bees (Apis mellifera L.): proboscis extension reflex (PER) studies. Insects, 5: 167-198. Go to original source... Go to PubMed...
  14. Delkash-Roudsari S., Chicas-Mosier A.M., Goldansaz S.H., Talebi-Jahromi K., Ashouri A., Abramson C.I. (2020): Assessment of lethal and sublethal effects of Imidacloprid, ethion, and glyphosate on aversive conditioning, motility, and lifespan in honey bees (Apis mellifera L.). Ecotoxicology and Environmental Safety, 204: 111108. Go to original source... Go to PubMed...
  15. Faghani M., Rahimian Y. (2018): Effect of glyphosate on honey bee (Apis mellifera) performance. Arthropods, 7: 77-81.
  16. Faita M.R., Oliveira E.M., Alves V.V., Orth A.I., Nodari R.O. (2018): Changes in hypopharyngeal glands of nurse bees (Apis mellifera) induced by pollen-containing sublethal doses of the herbicide Roundup®. Chemosphere, 211: 566-572. Go to original source... Go to PubMed...
  17. Farina W.M., Balbuena M.S., Herbert L.T., Mengoni Goñalons C., Vázquez D.E. (2019): Effects of the herbicide glyphosate on honey bee sensory and cognitive abilities: individual impairments with implications for the hive. Insects, 10: 354. Go to original source... Go to PubMed...
  18. García-Espiñeira M., Tejeda-Benitez L., Olivero-Verbel J. (2018): Toxicity of atrazine- and glyphosate-based formulations on Caenorhabditis elegans. Ecotoxicology and Environmental Safety, 156: 216-222. Go to original source... Go to PubMed...
  19. Giesy J.P., Dobson S., Solomon K.R. (2000): Ecotoxicological risk assessment for Roundup® herbicide. Reviews of Environmental Contamination and Toxicology, 167: 35-120. Go to original source...
  20. Glinski Z., Marc M., Chelminski A. (2012): Role of Varroa destructor as immunosuppressor and vector of infections in colony collapse disorder (CCD). Medycyna Weterynaryjna, 68: 585-588.
  21. Goldsborough L.G., Brown D.J. (1988): Effect of glyphosate (Roundup formulation) on periphytic algal photosynthesis. Bulletin of Environmental Contamination and Toxicology, 41: 253-260. Go to original source... Go to PubMed...
  22. Goñalons C.M., Farina W.M. (2018): Impaired associative learning after chronic exposure to pesticides in young adult honey bees. Journal of Experimental Biology, 221: 176644. Go to original source... Go to PubMed...
  23. Gray A., Adjlane N., Arab A., Ballis A., Brusbardis V., Charrière J.D., Chlebo R., Coffey M.F., Cornelissen B., Amaro da Costa C., Dahle B., Danihlík J., Dra¾iæ M.M., Evans G., Fedoriak M., Forsythe I., Gajda A., de Graaf D.C., Gregorc A., Ilieva I., Johannesen J., Kauko L., Kristiansen P., Martikkala M., Martín-Hernández R., Medina-Flores C.A., Mutinelli F., Patalano S., Raudmets A., San Martin G., Soroker V., Stevanovic J., Uzunov A., Vejsnaes F., Williams A., Zammit-Mangion M., Brodschneider R. (2020): Honey bee colony winter loss rates for 35 countries participating in the COLOSS survey for winter 2018-2019, and the effects of a new queen on the risk of colony winter loss. Journal of Apicultural Research, 59: 744-751. Go to original source...
  24. Grüter C., Farina W.M. (2007): Nectar distribution and its relation to food quality in honeybee (Apis mellifera) colonies. Insectes Sociaux, 54: 87-94. Go to original source...
  25. Henry M., Béguin M., Requier F., Rollin O., Odoux J.F., Aupinel P., Aptel J., Tchamitchian S., Decourtye A. (2012): A common pesticide decreases foraging success and survival in honey bees. Science, 336: 348-350. Go to original source... Go to PubMed...
  26. Herbert L.T., Vázquez D.E., Arenas A., Farina W.M. (2014): Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour. Journal of Experimental Biology, 217: 3457-3464. Go to original source... Go to PubMed...
  27. Janssens L., Stoks R. (2017): Stronger effects of Roundup than its active ingredient glyphosate in damselfly larvae. Aquatic Toxicology, 193: 210-216. Go to original source... Go to PubMed...
  28. Jolodar N.R., Karimi S., Bouteh E., Balist J., Prosser R. (2021): Human health and ecological risk assessment of pesticides from rice production in the Babol Roud River in Northern Iran. Science of the Total Environment, 772: 144729. Go to original source... Go to PubMed...
  29. Kaplan J.K. (2008): Colony collapse disorder. A complex buzz. Agricultural Research, 56: 8-11.
  30. Karahan A., Çakmak I., Hranitz J.M., Karaca I., Wells H. (2015): Sublethal Imidacloprid effects on honey bee flower choices when foraging. Ecotoxicology, 24: 2017-2025. Go to original source... Go to PubMed...
  31. 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. Go to original source... Go to PubMed...
  32. Kulincevic J.M., Rothenbuhler W.C., Rinderer T.E. (1982): Disappearing disease. Part 1 - effects of certain protein sources given to honey bee colonies in Florida. American Bee Journal, 122: 191-198.
  33. Lambert O., Piroux M., Puyo S., Thorin C., L'Hostis M., Wiest L., Buleté A., Delbac F., Pouliquen H. (2013): Widespread occurrence of chemical residues in beehive matrices from apiaries located in different landscapes of Western France. PLOS One, 8: e67007. Go to original source... Go to PubMed...
  34. Lima I.S., Pinto K.D.S., Franca F.B., Brighenti C.R.G., Serpa D.C., Brighenti D.M. (2019): Bayesian approach of the logistic model in the study of glyphosate herbicide in bees. Sigmae, 8: 282-289.
  35. Lu C.H.A., Warchol K.M., Callahan R.A. (2012): In situ replication of honey bee colony collapse disorder. Bulletin of Insectology, 65: 99-106.
  36. Luo Q.H., Gao J., Guo Y., Liu C., Ma Y.Z., Zhou Z.Y., Dai P.L., Hou C.S., Wu Y.Y., Diao Q.Y. (2021): Effects of a commercially formulated glyphosate solutions at recommended concentrations on honeybee (Apis mellifera L.) behaviours. Scientific Reports, 11: 2115. Go to original source... Go to PubMed...
  37. Menzel R. (2012): The honeybee as a model for understanding the basis of cognition. Nature Reviews Neuroscience, 13: 758-768. Go to original source... Go to PubMed...
  38. Menzel R. (1999): Memory dynamics in the honeybee. Journal of Comparative Physiology A, 185: 323-340. Go to original source...
  39. Michalkova V., Pekar S. (2009): How glyphosate altered the behaviour of agrobiont spiders (Araneae: Lycosidae) and beetles (Coleoptera: Carabidae). Biological Control, 51: 444-449. Go to original source...
  40. Morvillo M. (2020): Glyphosate effect: has the glyphosate controversy affected the EU's regulatory epistemology? European Journal of Risk Regulation, 11: 422-435. Go to original source...
  41. Motta E.V.S., Moran N.A. (2020): Impact of glyphosate on the honey bee gut microbiota: effects of intensity, duration, and timing of exposure. mSystems, 5: e00268-20. Go to original source... Go to PubMed...
  42. Motta E.V.S., Raymann K., Moran N.A. (2018): Glyphosate perturbs the gut microbiota of honey bees. Proceedings of the National Academy of Sciences of the United States of America, 115: 10305-10310. Go to original source... Go to PubMed...
  43. Mullin C.A., Frazier M., Frazier J.L., Ashcraft S., Simonds R., Vanengelsdorp D., Pettis J.S. (2010): High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLOS One, 5: e9754. Go to original source... Go to PubMed...
  44. Muñoz J.P., Bleak T.C., Calaf G.M. (2021): Glyphosate and the key characteristics of an endocrine disruptor: a review. Chemosphere, 270: 128619. Go to original source... Go to PubMed...
  45. Peghaire E., Moné A., Delbac F., Debroas D., Chaucheyras-Durand F., El Alaoui H. (2020): A Pediococcus strain to rescue honeybees by decreasing Nosema ceranae- and pesticide-induced adverse effects. Pesticide Biochemistry and Physiology, 163: 138-146. Go to original source... Go to PubMed...
  46. Pohorecka K., Skubida P., Miszczak A., Semkiw P., Sikorski P., Zagibaj³o K., Teper D., Koltowski Z., Skubida M., Zdañska D., Bober A. (2012): Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. Journal of Apicultural Science, 56: 115-134. Go to original source...
  47. Qu R.Y., He B., Yang J.F., Lin H.Y., Yang W.C., Wu Q.Y., Li Q.X., Yang G.F. (2021): Where are the new herbicides? Pest Management Science, 77: 2620-2625. Go to original source... Go to PubMed...
  48. Richmond M.E. (2018): Glyphosate: a review of its global use, environmental impact, and potential health effects on humans and other species. Journal of Environmental Studies and Sciences, 8: 416-434. Go to original source...
  49. Rossi A.S., Fantón N., Michlig M.P., Repetti M.R., Cazenave J. (2020): Fish inhabiting rice fields: bioaccumulation, oxidative stress and neurotoxic effects after pesticides application. Ecological Indicators, 113: 106186. Go to original source...
  50. Rubio F., Guo E., Kamp L. (2014): Survey of glyphosate residues in honey, corn and soy products. Journal of Environmental and Analytical Toxicology, 5: 249.
  51. Shefali G., Kumar R.R., Sankhla M.S., Kumar R., Sonone S.S. (2021): Impact of pesticide toxicity in aquatic environment. Biointerface Research in Applied Chemistry, 11: 10131-10140. Go to original source...
  52. Sviridov A.V., Shushkova T.V., Ermakova I.T., Ivanova E.V., Epiktetov D.O., Leont'evskii A.A. (2015): Microbial degradation of glyphosate herbicides (Review). Applied Biochemistry and Microbiology, 51: 188-195. Go to original source...
  53. Thompson H.M., Levine S.L., Doering J., Norman S., Manson P., Sutton P., von Mérey G. (2014): Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example. Integrated Environmental Assessment and Management, 10: 463-470. Go to original source... Go to PubMed...
  54. Tran N., Drogui P., Doan T.L., Le T.S., Nguyen H.C. (2017): Electrochemical degradation and mineralization of glyphosate herbicide. Environmental Technology, 38: 2939-2948. Go to original source... Go to PubMed...
  55. United States Environmental Protection Agency (2017): Pesticides industry sales and usage 2008-2012 market estimates. Washington, United States Environmental Protection Agency, 1-24.
  56. Villamar-Ayala C.A., Carrera-Cevallos J.V., Vasquez-Medrano R., Espinoza-Montero P.J. (2019): Fate, eco-toxicological characteristics, and treatment processes applied to water polluted with glyphosate: a critical review. Critical Reviews in Environmental Science and Technology, 49: 1476-1514. Go to original source...
  57. Wilmart O., Legrève A., Scippo M.L., Reybroeck W., Urbain B., de Graaf D.C., Spanoghe P., Delahaut P., Saegerman C. (2021): Honey bee exposure scenarios to selected residues through contaminated beeswax. Science of the Total Environment, 772: 145533. Go to original source... Go to PubMed...
  58. Zaluski R., Kadri S.M., Alonso D.P., Martins Ribolla P.E., de Oliveira Orsi R. (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. Go to original source... Go to PubMed...
  59. Zhang W., Jiang F., Ou J. (2011): Global pesticide consumption and pollution: with China as a focus. Proceedings of the International Academy of Ecology and Environmental Sciences, 1: 125-144. Go to original source...
  60. Zioga E., Kelly R., White B., Stout J.C. (2020): Plant protection product residues in plant pollen and nectar: a review of current knowledge. Environmental Research, 189: 109873. Go to original source... Go to PubMed...

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