Scippo, Marie-Louise ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
Reybroeck, Wim
Urbain, Bruno
de Graaf, Dirk C.
Spanoghe, Pieter
Delahaut, Philippe
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 :
Honey bee exposure scenarios to selected residues through contaminated beeswax
ANSES, Co-exposition des abeilles aux facteurs de stress. Avis de l'ANSES. Rapport d'expertise collective. Saisine n° 2012-SA-0176. ANSES (Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail). 252 p https://www.anses.fr/fr/system/files/SANT2012sa0176Ra.pdf, 2015.
Aupinel, P., Fortini, D., Dufour, H., Tasei, J., Michaud, B., Odoux, F., Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bull. Insectol. 58:2 (2005), 107–111 http://www.bulletinofinsectology.org/pdfarticles/vol58-2005-107-111aupinel.pdf.
Babendreier, D., Kalberer, N., Romeis, J., Fluri, P., Bigler, F., Pollen consumption in honey bee larvae: a step forward in the risk assessment of transgenic plants. Apidologie. 35:3 (2004), 293–300, 10.1051/apido:2004016.
Bauer, D., Bienefeld, K., Hexagonal comb cells of honeybees are not produced via a liquid equilibrium process. Naturwissenschaften. 100 (2013), 45–49, 10.1007/s00114-012-0992-3.
Boecking, O., Genersch, E., Varroosis – the ongoing crisis in bee keeping. J. Verbr. Lebensm. 3 (2008), 221–228, 10.1007/s00003-008-0331-y.
Bogdanov, S., Royal Jelly, Bee Brood: Composition, Health, Medicine: A Review. 2017, Bee Product Science.
Bogdanov, S., Kilchenmann, V., Imdorf, A., Acaricide residues in some bee products. J. Apic. Res. 37:2 (1998), 57–67, 10.1080/00218839.1998.11100956.
Böhme, F., Bischoff, G., Zebitz, C.P.W., 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, 13(7), 2018, e0199995, 10.1371/journal.pone.0199995.
Boi, M., Serra, G., Colombo, R., Lodesani, M., Massi, S., Costa, C., A 10 year survey of acaricide residues in beeswax analysed in Italy. Pest Manag. Sci. 72:7 (2016), 1366–1372, 10.1002/ps.4161.
Brodschneider, R., Crailsheim, K., Nutrition and health in honey bees. Apidologie. 41:3 (2010), 278–294, 10.1051/apido/2010012.
Calatayud-Vernich, P., Calatayud, F., Simó, E., Picó, E., Occurrence of pesticide residues in Spanish beeswax. Sci. Total Environ. 605–606:2017 (2017), 745–754, 10.1016/j.scitotenv.2017.06.174.
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.
Charpentier, G., Vidau, C., Ferdy, J.B., Tabart, J., Vetillard, A., Lethal and sub-lethal effects of thymol on honeybee (Apis mellifera) larvae reared in vitro. Pest Manag. Sci. 70:1 (2014), 140–147, 10.1002/ps.3539.
Chauzat, M.P., Faucon, J.P., Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in France. Pest Manag. Sci. 63:11 (2007), 1100–1106, 10.1002/ps.1451.
Colin, M.-E., Belzunces, L.P., Evidence of synergy between prochloraz and deltamethrin in Apis mellifera L.: a convenient biological approach. Pestic. Sci. 36:2 (1992), 115–119, 10.1002/ps.2780360206.
Cornman, R.S., Tarpy, D.R., Chen, Y., Jeffreys, L., Lopez, D., Pettis, J.S., vanEngelsdorp, D., Evans, J.D., Pathogen webs in collapsing honey bee colonies. PLoS One, 7(8), 2012, e43562, 10.1371/journal.pone.0043562.
Crailsheim, K., Brodschneider, R., Aupinel, P., Behrens, D., Genersch, E., Vollmann, J., Riessberger-Gallé, U., Standard methods for artificial rearing of Apis mellifera larvae. J. Apic. Res. 52:1 (2013), 1–16, 10.3896/IBRA.1.52.1.05.
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. 73:11 (2017), 2282–2286, 10.1002/ps.4608.
Dai, P., Jack, C.J., Mortensen, A.N., Bustamante, T.A., Ellis, J.D., Chronic toxicity of amitraz, coumaphos and fluvalinate to Apis mellifera L. larvae reared in vitro. Sci. Rep., 8(1), 2018, 5635, 10.1038/s41598-018-24045-3.
Dai, P., Jack, C.J., Mortensen, A.N., Bustamante, T.A., Bloomquist, J.R., Ellis, J.D., Chronic toxicity of clothianidin, imidacloprid, chlorpyrifos, and dimethoate to Apis mellifera L. larvae reared in vitro. Pest Manag. Sci. 75:1 (2019), 29–36, 10.1002/ps.5124.
Daniele, G., Giroud, B., Jabot, C., Vulliet, E., Exposure assessment of honeybees through study of hive matrices: analysis of selected pesticide residues in honeybees, beebread, and beeswax from French beehives by LC-MS/MS. Environ. Sci. Pollut. Res. 25 (2018), 6145–6153, 10.1007/s11356-017-9227-7.
EFSA, Risk assessment of beeswax adulterated with paraffin and/or stearin/stearic acid when used in apiculture and as food (honeycomb). EFSA Support. Publ., 2020, 10.2903/sp.efsa.2020.EN-1859 2020:17(5):EN-1859.
El Agrebi, N., Wilmart, O., Urbain, B., Danneels, E.L., de Graaf, D.C., Saegerman, C., Belgian case study on flumethrin residues in beeswax: possible impact on honeybee and prediction of the maximum daily intake for consumers. Sci. Total Environ. 687:2019 (2019), 712–719, 10.1016/j.scitotenv.2019.05.493.
El Agrebi, N., Tosi, S., Wilmart, O., Scippo, M.-L., de Graaf, D.C., Saegerman, C., Honeybee and consumer's exposure and risk characterisation to glyphosate-based herbicide (GBH) and its degradation product (AMPA): residues in beebread, wax, and honey. Sci. Total Environ., 704(2020), 2020, 135312, 10.1016/j.scitotenv.2019.135312.
El Agrebi, N., Traynor, K., Wilmart, O., Tosi, S., Leinartz, L., Danneels, E., de Graaf, D.C., Saegerman, C., Pesticide and veterinary drug residues in Belgian beeswax: occurrence, toxicity, and risk to honey bees. Sci. Total Environ., 745(2020), 2020, 141036, 10.1016/j.scitotenv.2020.141036.
Fulton, C.A., Huff Hartz, K.E., Reeve, J.D., Lydy, M.J., An examination of exposure routes of fluvalinate to larval and adult honey bees (Apis mellifera). Environ. Toxicol. Chem. 38 (2019), 1356–1363, 10.1002/etc.4427.
Ghosh, S., Jung, C., Meyer-Rochow, V.B., Nutritional value and chemical composition of larvae, pupae, and adults of worker honey bee, Apis mellifera ligustica as a sustainable food source. J. Asia Pac. Entomol. 19:2 (2016), 487–495, 10.1016/j.aspen.2016.03.008.
Haydak, M.H., Larval food and development of castes in the honeybee. J. Econ. Entomol. 36:5 (1943), 778–792, 10.1093/jee/36.5.778.
Hepburn, H.R., Bernard, R.T.F., Davidson, B.C., Muller, W.J., Llyod, P., Kurstjens, S.P., Vincent, S.L., Synthesis and secretion of beeswax in honeybees. Apidologie. 22 (1991), 21–36, 10.1051/apido:19910104.
Hepburn, H.R., Pirk, C.W.W., Duangphakdee, O., Honeybee Nests: Composition, Structure, Function. 2014, Springer-Verlag, Berlin Heidelberg 389 p. (ISBN:978-3-642-54327-2).
Herrera López, S., Lozano, A., Sosa, A., Hernando, M.D., Fernández-Alba, A.R., Screening of pesticide residues in honeybee wax comb by LC-ESI-MS/MS. A pilot study. Chemosphere. 163:2016 (2016), 44–53, 10.1016/j.chemosphere.2016.07.008.
Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A.V., García-Palencia, P., Meana, A., Del Nozal, M.J., Mayo, R., Bernal, J.L., Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ. Microbiol. Rep. 1 (2009), 110–113, 10.1111/j.1758-2229.2009.00014.x.
HMA, Authorised bee products: situation in Europe. EMA/CMDv/497311/2009 rev. 15. Co-ordination Group for Mutual Recognition and Decentralised Procedures – Veterinary (CMDVv), 2019, European Medicines Agency (EMA) https://www.hma.eu/fileadmin/dateien/Veterinary_medicines/CMDv_Website/Procedural_guidance/Miscellaneous/Bee_products_available_in_Europe2019.pdf.
Johnson, R.M., Pollock, H.S., Berenbaum, M.R., Synergistic interactions between in-hive miticides in Apis mellifera. J. Econ. Entomol. 102:2 (2009), 474–479, 10.1603/029.102.0202.
Johnson, R.M., Dahlgren, L., Siegfried, B.D., Ellis, M.D., Acaricide, fungicide and drug interactions in honey bees (apis mellifera). PLoS One, 8(1), 2013, e54092, 10.1371/journal.pone.0054092.
Johnson, R.M., Ellis, M.D., Mullin, C.A., Frazier, M., Pesticides and honey bee toxicity – USA. Apidologie. 41:2010 (2010), 312–331, 10.1051/apido/2010018.
Kast, C., Kilchenmann, V., Droz, B., Distribution of coumaphos in beeswax after treatment of honeybee colonies with CheckMite® against the parasitical mite Varroa destructor. Apidologie. 51 (2020), 112–122, 10.1007/s13592-019-00724-6.
Lozano, A., Hernando, M.D., Uclés, S., Hakme, E., Fernández-Alba, A.R., Identification and measurement of veterinary drug residues in beehive products. Food Chem. 274:2019 (2019), 61–70, 10.1016/j.foodchem.2018.08.055.
Martel, A.-C., Zeggane, S., Aurières, C., Drajnudel, P., Faucon, J.-P., Aubert, M., Acaricide residues in honey and wax after treatment of honey bee colonies with Apivar® or Asuntol®50. Apidologie. 38:06 (2007), 534–544, 10.1051/apido:2007038.
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(3), 2010, e9754, 10.1371/journal.pone.0009754.
OECD, MRL Calculator: Users Guide and White Paper, Series on Pesticides and Biocides, No. 56. 2014, OECD Publishing, Paris, 10.1787/9789264221567-en.
OECD, Test no. 213: honeybees, acute oral toxicity test. Guidelines for the testing of chemicals, section 2: effects on biotic systems. https://www.oecd-ilibrary.org/environment/test-no-213-honeybees-acute-oral-toxicity-test_9789264070165-en, 1998.
OECD, Test no. 214: honeybees, acute contact toxicity test. Guidelines for the testing of chemicals, section 2: effects on biotic systems. https://www.oecd-ilibrary.org/environment/test-no-214-honeybees-acute-contact-toxicity-test_9789264070189-en, 1998.
Oruc, H.H., Hranitz, J.M., Sorucu, A., Duell, M., Cakmak, I., Aydin, L., Orman, A., Determination of acute oral toxicity of flumethrin in honey bees. J. Econ. Entomol. 105:6 (2012), 1890–1894, 10.1603/EC12055.
Ostiguy, N., Drummond, F.A., Aronstein, K., Eitzer, B., Ellis, J.D., Spivak, M., Sheppard, W.S., Honey bee exposure to pesticides: a four-year nationwide study. Insects, 10(01), 2019, 13, 10.3390/insects10010013.
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 (2018), 470–476, 10.1016/j.scitotenv.2017.12.321.
Piechowicz, B., Woś, I., Podbielska, M., Grodzicki, P., The transfer of active ingredients of insecticides and fungicides from an orchard to beehives. J. Environ. Sci. Health B 53:1 (2018), 18–24, 10.1080/03601234.2017.1369320.
Pilling, E.D., Bromley-Challenor, K.A.C., Walker, C.H., Jepson, P.C., Mechanism of synergism between the pyrethroid insecticide λ-cyhalothrin and the imidazole fungicide prochloraz, in the honeybee (Apis mellifera L.). Pestic. Biochem. Physiol. 51:1 (1995), 1–11, 10.1006/pest.1995.1001.
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.
Rembold, H., Dietz, A., Biologically active substances in royal jelly. Vitam. Hormones 23 (1966), 359–382, 10.1016/S0083-6729(08)60385-4.
Rembold, H., Lackner, B., Rearing of honeybee larvae in vitro: effect of yeast extract on queen differentiation. J. Apic. Res. 20:3 (1981), 165–171, 10.1080/00218839.1981.11100492.
Rortais, A., Villemant, C., Gargominy, O., Rome, Q., Haxaire, J., Papachristoforou, A., Arnold, G., A new enemy of honeybees in Europe: the Asian hornet Vespa velutina. Settele, J., Penev, L.D., Georgiev, T.A., Grabaum, R., Grobelnik, V., Hammen, V., Klotz, S., Kotarac, M., Kühn, I., (eds.) Atlas of Biodiversit Risk. Chapter: 7. Decline of Pollinators and Its Impact, 2010, Pensoft Publishers 264p. (ISBN: 9789546424464).
Rortais, A., Arnold, G., Dorne, J.-L., More, S.J., Sperandio, G., Streissl, F., Szentes, C., Verdonck, F., Risk assessment of pesticides and other stressors in bees: principles, data gaps and perspectives from the European Food Safety Authority. Sci. Total Environ. 587–588:2017 (2017), 524–537, 10.1016/j.scitotenv.2016.09.127.
Rosenkranz, P., Aumeier, P., Ziegelmann, B., Biology and control of Varroa destructor. J. Invertebr. Pathol. 103:2010 (2010), S96–S119, 10.1016/j.jip.2009.07.016.
Sánchez-Bayo, F., Goka, K., Pesticide residues and bees – a risk assessment. PLoS One, 9(4), 2014, e94482, 10.1371/journal.pone.0094482.
Sánchez-Bayo, F., Goulson, D., Pennacchio, F., Nazzi, F., Goka, K., Desneux, N., Are bee diseases linked to pesticides? — a brief review. Environ. Int. 89–90:2016 (2016), 7–11, 10.1016/j.envint.2016.01.009.
Schmehl, D.R., Tomé, H.V.V., Mortensen, A.N., Martins, G.F., Ellis, J.D., Protocol for the in vitro rearing of honey bee (Apis mellifera L.) workers. J. Apic. Res. 55:2 (2016), 113–129, 10.1080/00218839.2016.1203530.
SciCom, Advice 18-2018 of the Scientific Committee of the FASFC Regarding the Risk to Bee Health of Contaminated and Adulterated Beeswax (SciCom 2016/27). Brussels, 14th November 2018. Full text only available in French http://www.favv-afsca.fgov.be/comitescientifique/avis/2018/_documents/Avis18-2018_SciCom2016-27_residus_cire_santeabeilles.pdf, 2018 or in Dutch http://www.favv-afsca.fgov.be/wetenschappelijkcomite/adviezen/2018/_documents/Advies18-2018_SciCom2016-27_residuen_bijenwas_bijengezondheid.pdf.
Serra-Bonvehí, J., Orantes-Bermejo, J., Acaricides and their residues in Spanish commercial beeswax. Pest Manag. Sci. 66:11 (2010), 1230–1235, 10.1002/ps.1999.
Shi, J., Zhang, R., Pei, Y., Liao, C., Wu, X., Exposure to acetamiprid influences the development and survival ability of worker bees (Apis mellifera L.) from larvae to adults. Environ. Pollut., 266(2020), 2020, 115345, 10.1016/j.envpol.2020.115345.
Shimshoni, J.A., Sperling, R., Massarwa, M., Chen, Y., Bommuraj, V., Borisover, M., Barel, S., Pesticide distribution and depletion kinetic determination in honey and beeswax: model for pesticide occurrence and distribution in beehive products. PLoS One, 14(2), 2019, e0212631, 10.1371/journal.pone.0212631.
Simon-Delso, N., San Martin, G., Bruneau, E., Minsart, L.-A., Mouret, C., Hautier, L., Honeybee colony disorder in crop areas: the role of pesticides and viruses. PLoS One, 9(7), 2014, e103073, 10.1371/journal.pone.0103073.
Snodgrass, R.E., The Anatomy of the Honey Bee. Technical Series, No. 18. United States. Dept. of Agriculture. Bureau of Entomology. 1910, Government Printing Office, Washington, 10.5962/bhl.title.87234.
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(10), 2013, e77550, 10.1371/journal.pone.0077550.
Tavares, D.A., Dussaubat, C., Kretzschmar, A., Carvalho, S.M., Silva-Zacarin, E.C.M., Malaspina, O., Bérail, G., Brunet, J.L., Belzunces, L.P., Exposure of larvae to thiamethoxam affects the survival and physiology of the honey bee at post-embryonic stages. Environ. Pollut. 229 (2017), 386–393, 10.1016/j.envpol.2017.05.092.
Thompson, H.M., Interaction between pesticides and other factors in effects on bees. EFSA Support. Publ., 2012, 10.2903/sp.efsa.2012.EN-340 2012:EN-340.
Tong, Z., Duan, J., Wu, Y., Liu, Q., He, Q., Shi, Y., Yu, L., Cao, H., A survey of multiple pesticide residues in pollen and beebread collected in China. Sci. Total Environ. 640–641:2018 (2018), 1578–1586, 10.1016/j.scitotenv.2018.04.424.
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.
Vandenberg, J.D., Shimanuki, H., Technique for rearing worker honeybees in the laboratory. J. Apic. Res. 26:2 (1987), 90–97, 10.1080/00218839.1987.11100743.
Wade, A., Lin, C.-H., Kurkul, C., Regan, E.R., Johnson, R.M., Combined toxicity of insecticides and fungicides applied to California almond orchards to honey bee larvae and adults. Insects, 10(01), 2019, 20, 10.3390/insects10010020.
Wallner, K., Varroacides and their residues in bee products. Apidologie. 30:1999 (1999), 235–248, 10.1051/apido:19990212.
Wang, Y., Zhu, Y.C., Li, W., Interaction patterns and combined toxic effects of acetamiprid in combination with seven pesticides on honey bee (Apis mellifera L.). Ecotoxicol. Environ. Saf., 190(2020), 2020, 110100, 10.1016/j.ecoenv.2019.110100.
Wilmart, O., Legrève, A., Scippo, M.-L., Reybroeck, W., Urbain, B., de Graaf, D.C., Steurbaut, W., Delahaut, P., Gustin, P., Nguyen, B.K., Saegerman, C., Residues in beeswax: a health risk for the consumer of honey and beeswax?. J. Agric. Food Chem. 64:44 (2016), 8425–8434 https://pubs.acs.org/doi/10.1021/acs.jafc.6b02813.
Winston, M.L., The Biology of the Honey Bee. 1987, Harvard University Press, Cambridge, Mass 281 p. (ISBN:0674074084).
Wright, G.A., Nicolson, S.W., Shafir, S., Nutritional physiology and ecology of honey bees. Annu. Rev. Entomol. 63:1 (2018), 327–344, 10.1146/annurev-ento-020117-043423.
Wu, J.Y., Smart, M.D., Anelli, C.M., Sheppard, W.S., Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. J. Invertebr. Pathol. 109:2012 (2012), 326–329, 10.1016/j.jip.2012.01.005.
Yao, J., Zhu, Y.C., Adamczyk, J., Responses of honey bees to lethal and sublethal doses of formulated clothianidin alone and mixtures. J. Econ. Entomol. 111:4 (2018), 1517–1525, 10.1093/jee/toy140.
Zhu, W., Schmehl, D.R., Mullin, C.A., Frazier, J.L., Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLoS One, 9(1), 2014, e77547, 10.1371/journal.pone.0077547.
