Honeybee and consumer’s exposure and risk characterisation to glyphosate-based herbicide (GBH) and its degradation product (AMPA): Residues in beebread, wax, and honey
El Agrebi, Noémie; Tosi, Simone; Wilmart, Olivieret al.
2020 • In Science of the Total Environment, 704, p. 135312
Scippo, Marie-Louise ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
de Graaf, Dirk
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appl. aux sc. vétér.
Language :
English
Title :
Honeybee and consumer’s exposure and risk characterisation to glyphosate-based herbicide (GBH) and its degradation product (AMPA): Residues in beebread, wax, and honey
Aizen, M.A., Garibaldi, L.A., Cunningham, S.A., Klein, A.M., How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann. Bot. 103 (2009), 1579–1588, 10.1093/aob/mcp076.
Aktar, W., Sengupta, D., Chowdhury, A., Impact of pesticides use in agriculture: Their benefits and hazards. Interdiscip. Toxicol. 2 (2009), 1–12, 10.2478/v10102-009-0001-7.
Arregui, M.C., Lenardón, A., Sanchez, D., Maitre, M.I., Scotta, R., Enrique, S., Monitoring glyphosate residues in transgenic glyphosate-resistant soybean. Pest Manag. Sci. 60 (2004), 163–166, 10.1002/ps.775.
Atkins, E.L., Kellum, D., Atkins, K.W., 1981. Reducing pesticide hazards to honey bees: mortality prediction techniques and integrated management strategies. Leafl. - Univ. California, Coop. Ext. Serv.
Balbuena, T.L., Hahn, M.L., Greggers, U., Menzel, R., Farina, W.M., Effects of sublethal doses of glyphosate on honeybee navigation. J. Exp. Biol. 218 (2015), 2799–2805, 10.1242/jeb.117291.
Benbrook, C.M., Trends in glyphosate herbicide use in the United States and globally. Environ. Sci. Eur., 28, 2016, 3, 10.1186/s12302-016-0070-0.
Blot, N., Veillat, L., Rouzé, R., Delatte, H., Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota. PLoS One, 14, 2019, e0215466, 10.1371/journal.pone.0215466.
Boily, M., Sarrasin, B., DeBlois, C., Aras, P., Chagnon, M., Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids, atrazine and glyphosate: laboratory and field experiments. Environ. Sci. Pollut. Res. 20 (2013), 5603–5614, 10.1007/s11356-013-1568-2.
Bonzini, S., Tremolada, P., Bernardinelli, I., Colombo, M., Vighi, M., Predicting pesticide fate in the hive (part 1): Experimentally determined τ-Fluvalinate residues in bees, honey and wax. Apidologie 42 (2011), 378–390, 10.1007/s13592-011-0011-2.
Bruggen, V.J. Jr, Environmental and health effects of the herbicide glyphosate. Sci. Total Environ. 616617 (2017), 255–268, 10.1016/j.scitotenv.2017.10.309.
Calatayud-Vernich, P., Calatayud, F., Simó, E., Picó, Y., Pesticide residues in honey bees, pollen and beeswax: Assessing beehive exposure. Environ. Pollut. 241 (2018), 106–114, 10.1016/J.ENVPOL.2018.05.062.
Chauzat, M.-P., Faucon, J.-P., Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in France. Pest Manag. Sci. 63 (2007), 1100–1106, 10.1002/ps.1451.
Conclusion on the peer review of the pesticide risk assessment of the active substance glyphosate, 2015. EFSA J. 13. doi:10.2903/j.efsa.2015.4302.
Dai, P., Jack, C.J., Mortensen, A.N., Ellis, J.D., Acute toxicity of five pesticides to Apis mellifera larvae reared in vitro. Pest Manag. Sci. 73 (2017), 2282–2286, 10.1002/ps.4608.
Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L.P., Decourtye, A., Kretzschmar, A., Suchail, S., Brunet, J.L., Alaux, C., Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter?. PLoS One 8 (2013), 1–14, 10.1371/journal.pone.0072016.
Dill, G.M., Sammons, R.D., Feng, P.C.C., Kohn, F., Kretzmer, K., Mehrsheikh, A., Bleeke, M., Honegger, J.L., Farmer, D., Wright, D., Haupfear, E.A., Glyphosate: discovery, development, applications, and properties. Glyphosate Resistance in Crops and Weeds, 2010, John Wiley & Sons, Inc., Hoboken, NJ, USA, 1–33, 10.1002/9780470634394.ch1.
Duke, S.O., Powles, S.B., Glyphosate: a once-in-a-century herbicide. Pest Manag. Sci. 64 (2008), 319–325, 10.1002/ps.1518.
EFSA, 2018. The EFSA Comprehensive European Food Consumption Database [WWW Document]. URL http://data.europa.eu/euodp/data/dataset/the-efsa-comprehensive-european-food-consumption-database (accessed 6.5.19).
EFSA, Beeswax (E 901) as a glazing agent and as carrier for flavours scientific opinion of the panel on food additives, flavourings, processing aids and materials in contact with food (AFC). EFSA J. 615 (2007), 1–28.
EPA, 1997. Pesticide regulation notice 97-6. Use of the term “inert” in the label ingredients statement.
European Commission, 2016. EU regulation No. 1107/2009. doi:10.1590/S0085-56262014000100008.
European Commission, 2002. Review Report for the Active Substance Glyphosate (No. 6511/VI/99-final), Protection Directorate-general, Directorate E e Food Safety: Plant Health, Animal Health and Welfare, International Questions.
Faita, M.R., de Oliveira, E.M., Alves, V.V., Orth, A.I., Nodari, R.O., Changes in hypopharyngeal glands of nurse bees (Apis mellifera) induced by pollen-containing sublethal doses of the herbicide Roundup®. Chemosphere 211 (2018), 566–572, 10.1016/J.CHEMOSPHERE.2018.07.189.
Food, E., Authority, S., 2017. The 2015 European Union Report on Pesticide Residues in Food, EFSA Journal. doi:10.2903/j.efsa.2016.4611.
Fratini, F., Cilia, G., Turchi, B., Felicioli, A., Beeswax: A minireview of its antimicrobial activity and its application in medicine. Asian Pac. J. Trop. Med. 9 (2016), 839–843, 10.1016/J.APJTM.2016.07.003.
Giesy, J.P., Dobson, S., Solomon, K.R., Ecotoxicological Risk Assessment for Roundup® Herbicide. 2000, Springer, New York, NY, 35–120.
Grunewald, K., Schmidt, W., Unger, C., Hanschmann, G., Behavior of glyphosate and aminomethylphosphonic acid (AMPA) in soils and water of reservoir Radeburg II catchment (Saxony/Germany). J. Plant Nutr. Soil Sci. 164 (2001), 65–70, 10.1002/1522-2624(200102)164:1<65::AID-JPLN65>3.0.CO;2-G.
Helmer, S.H., Kerbaol, A., Aras, P., Jumarie, C., Boily, M., Effects of realistic doses of atrazine, metolachlor, and glyphosate on lipid peroxidation and diet-derived antioxidants in caged honey bees (Apis mellifera). Environ. Sci. Pollut. Res. 22 (2015), 8010–8021, 10.1007/s11356-014-2879-7.
Herbert, L.T., Vazquez, D.E., Arenas, A., Farina, W.M., Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour. J. Exp. Biol. 217 (2014), 3457–3464, 10.1242/jeb.109520.
ITSAP, 2017. Guide des bonnes pratiques apicoles.
Jumarie, C., Aras, P., Boily, M., Mixtures of herbicides and metals affect the redox system of honey bees. Chemosphere 168 (2017), 163–170, 10.1016/J.CHEMOSPHERE.2016.10.056.
Krupke, C.H., Hunt, G.J., Eitzer, B.D., Andino, G., Given, K., Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One, 7, 2012, e29268, 10.1371/journal.pone.0029268.
Lambert, O., Piroux, M., Puyo, S., Thorin, C., L'Hostis, M., Wiest, L., Buleté, A., Delbac, F., Pouliquen, H., Widespread occurrence of chemical residues in beehive matrices from apiaries located in different landscapes of Western France. PLoS One, 8, 2013, e67007, 10.1371/journal.pone.0067007.
Lewis, K.A., Tzilivakis, J., Warner, D.J., Green, A., An international database for pesticide risk assessments and management. Hum. Ecol. Risk Assess. 22 (2016), 1050–1064, 10.1080/10807039.2015.1133242.
Mamy, L., Barriuso, E., Gabrielle, B., Glyphosate fate in soils when arriving in plant residues. Chemosphere 154 (2016), 425–433, 10.1016/J.CHEMOSPHERE.2016.03.104.
Mañas, F., Peralta, L., Raviolo, J., García Ovando, H., Weyers, A., Ugnia, L., Gonzalez Cid, M., Larripa, I., Gorla, N., Genotoxicity of AMPA, the environmental metabolite of glyphosate, assessed by the Comet assay and cytogenetic tests. Ecotoxicol. Environ. Saf. 72 (2009), 834–837, 10.1016/J.ECOENV.2008.09.019.
Manning, R., Chemical residues in beebread, honey, pollen and wax samples collected from bee hives placed on canola crops in Western Australia. J. Apic. Res., 2018, 1–13, 10.1080/00218839.2018.1494889.
Mengoni Goñalons, C., Farina, W.M., Impaired associative learning after chronic exposure to pesticides in young adult honey bees. J. Exp. Biol., 221, 2018, jeb176644, 10.1242/jeb.176644.
Mesnage, R., Benbrook, C., Antoniou, M.N., Insight into the confusion over surfactant co-formulants in glyphosate-based herbicides. Food Chem. Toxicol. 128 (2019), 137–145, 10.1016/J.FCT.2019.03.053.
Mesnage, R., Bernay, B., Séralini, G.E., Ethoxylated adjuvants of glyphosate-based herbicides are active principles of human cell toxicity. Toxicology 313 (2013), 122–128, 10.1016/j.tox.2012.09.006.
Mesnage, R., Defarge, N., Spiroux de Vendômois, J., Séralini, G.E., Potential toxic effects of glyphosate and its commercial formulations below regulatory limits. Food Chem. Toxicol. 84 (2015), 133–153, 10.1016/J.FCT.2015.08.012.
Motta, E.V.S., Raymann, K., Moran, N.A., Glyphosate perturbs the gut microbiota of honey bees. Proc. Natl. Acad. Sci., 115, 2018, 10.1073/pnas.1803880115.
Mullin, C.A., Effects of ‘inactive’ ingredients on bees. Curr. Opin. Insect Sci. 10 (2015), 194–200, 10.1016/J.COIS.2015.05.006.
Mullin, C.A., Chen, J., Fine, J.D., Frazier, M.T., Frazier, J.L., The formulation makes the honey bee poison. Pestic. Biochem. Physiol. 120 (2015), 27–35, 10.1016/J.PESTBP.2014.12.026.
Mullin, C.A., Frazier, M., Frazier, J.L., Ashcraft, S., Simonds, R., vanEngelsdorp, D., Pettis, J.S., High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One, 5, 2010, e9754, 10.1371/journal.pone.0009754.
Myers, J.P., Antoniou, M.N., Blumberg, B., Carroll, L., Colborn, T., Everett, L.G., Hansen, M., Landrigan, P.J., Lanphear, B.P., Mesnage, R., Vandenberg, L.N., Vom Saal, F.S., Welshons, W.V., Benbrook, C.M., Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement. Environ. Health, 15, 2016, 19, 10.1186/s12940-016-0117-0.
OECD, 2017. Guideline 245 for the testing of chemicals. Honey bee (Apis mellifera L.), chronic oral toxicity test (10-day feeding), OECD/OCDE, OECD Guidelines for the Testing of Chemicals, Section 2. OECD Publishing. doi:10.1787/9789264284081-en.
OECD, 1998. Test No 214: Guidelines for the Testing of Chemicals 1–7.
Orantes-Bermejo, F.J., Pajuelo, A.G., Megías, M.M., Torres Fernández-Píñar, C., Pesticide residues in beeswax and beebread samples collected from honey bee colonies (Apis mellifera L.) in Spain. Possible implications for bee losses. J. Apic. Res. 48 (2010), 243–250, 10.3896/IBRA.1.49.3.03.
Perugini, M., Tulini, S.M.R., Zezza, D., Fenucci, S., Conte, A., Amorena, M., Occurrence of agrochemical residues in beeswax samples collected in Italy during 2013–2015. Sci. Total Environ. 625 (2018), 470–476, 10.1016/J.SCITOTENV.2017.12.321.
QGIS Geographic Information System, 2009. (accessed 1 July 2009).
Ravoet, J., Reybroeck, W., de Graaf, D.C., Pesticides for apicultural and/or agricultural application found in Belgian honey bee wax combs. Bull. Environ. Contam. Toxicol. 94 (2015), 543–548, 10.1007/s00128-015-1511-y.
Renwick, A.G., Pesticide residue analysis and its relationship to hazard characterisation (ADI/ARfD) and intake estimations (NEDI/NESTI). Pest Manag. Sci. 58 (2002), 1073–1082, 10.1002/ps.544.
Roberts, T.R., Hutson, D.H., Lee, P.W., Nicholls, P.H., Plimmer, J.R., (eds.) Metabolic Pathways of Agrochemicals, 1999, Royal Society of Chemistry, Cambridge, 10.1039/9781847551375.
Rortais, A., Arnold, G., Halm, M.-P., Touffet-Briens, F., Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36 (2005), 71–83, 10.1051/apido:2004071.
Rubio, F., Guo, E., Kamp, L., Survey of glyphosate residues in honey, corn and soy products. J. Environ. Anal. Toxicol. 05 (2014), 1–8, 10.4172/2161-0525.1000249.
Service Public de Wallonie, 2017. Estimation quantitative des utilisations de produits phytopharmaceutiques par les différents secteurs d ’activité.
Shokri, J., Nokhodchi, A., Dashbolaghi, A., Hassan-Zadeh, D., Ghafourian, T., Barzegar Jalali, M., The effect of surfactants on the skin penetration of diazepam. Int. J. Pharm. 228 (2001), 99–107, 10.1016/S0378-5173(01)00805-5.
Shushkova, T., Ermakova, I., Leontievsky, A., Glyphosate bioavailability in soil. Biodegradation 21 (2010), 403–410, 10.1007/s10532-009-9310-y.
Silva, V., Montanarella, L., Jones, A., Fernández-Ugalde, O., Mol, H.G.J., Ritsema, C.J., Geissen, V., Distribution of glyphosate and aminomethylphosphonic acid (AMPA) in agricultural topsoils of the European Union. Sci. Total Environ. 621 (2018), 1352–1359, 10.1016/j.scitotenv.2017.10.093.
Simon-Delso, N., San Martin, G., Bruneau, E., Delcourt, C., Hautier, L., The challenges of predicting pesticide exposure of honey bees at landscape level. Sci. Rep., 7, 2017, 3801, 10.1038/s41598-017-03467-5.
Singh, B., Singh, K., Microbial degradation of herbicides. Crit. Rev. Microbiol. 42 (2016), 245–261, 10.3109/1040841X.2014.929564.
Stoner, K.A., Eitzer, B.D., Using a hazard quotient to evaluate pesticide residues detected in pollen trapped from honey bees (Apis mellifera) in connecticut. PLoS One 8 (2013), 1–10, 10.1371/journal.pone.0077550.
Stoner, K.A., Eitzer, B.D., Pacini, E., Roe, R., Lambin, M., Using a hazard quotient to evaluate pesticide residues detected in pollen trapped from honey bees (Apis mellifera) in connecticut. PLoS One 8 (2013), 1–10, 10.1371/journal.pone.0077550.
Tosi, S., Costa, C., Vesco, U., Quaglia, G., Guido, G., A 3-year survey of Italian honey bee-collected pollen reveals widespread contamination by agricultural pesticides. Sci. Total Environ. 615 (2018), 208–218, 10.1016/J.SCITOTENV.2017.09.226.
Tosi, S., Nieh, J.C., Sgolastra, F., Cabbri, R., Medrzycki, P., Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees. Proc. R. Soc. B Biol. Sci., 284, 2017, 20171711, 10.1098/rspb.2017.1711.
Traynor, K.S., Pettis, J.S., Tarpy, D.R., Mullin, C.A., Frazier, J.L., Frazier, M., vanEngelsdorp, D., In-hive Pesticide Exposome: Assessing risks to migratory honey bees from in-hive pesticide contamination in the Eastern United States. Sci. Rep., 6, 2016, 33207, 10.1038/srep33207.
Tsui, M.T.K., Chu, L.M., Aquatic toxicity of glyphosate-based formulations: Comparison between different organisms and the effects of environmental factors. Chemosphere 52 (2003), 1189–1197, 10.1016/S0045-6535(03)00306-0.
Vázquez, D.E., Ilina, N., Pagano, E.A., Zavala, J.A., Farina, W.M., Glyphosate affects the larval development of honey bees depending on the susceptibility of colonies. PLoS One, 13, 2018, e0205074, 10.1371/journal.pone.0205074.
Vergaert, S., 2017. De gesloten waskringloop.
Williams, G.M., Kroes, R., Munro, I.C., Safety evaluation and risk assessment of the herbicide roundup and its active ingredient, glyphosate, for humans. Regul. Toxicol. Pharmacol. 31 (2000), 117–165, 10.1006/RTPH.1999.1371.
Zhang, C., Hu, X., Luo, J., Wu, Z., Wang, L., Li, B., Wang, Y., Sun, G., Zhang, C., Hu, X., Luo, J., Wu, Z., Wang, L., Li, B., Wang, Y., Sun, G., Degradation dynamics of glyphosate in different types of citrus orchard soils in China. Molecules 20 (2015), 1161–1175, 10.3390/molecules20011161.
Zhu, Y.C., Yao, J., Adamczyk, J., Luttrell, R., Feeding toxicity and impact of imidacloprid formulation and mixtures with six representative pesticides at residue concentrations on honey bee physiology (Apis mellifera). PLoS One, 12, 2017, e0178421, 10.1371/journal.pone.0178421.
