Pesticide residue profiles in bee bread and pollen samples and the survival of honeybee colonies—a case study from Luxembourg
Pesticide residues (112 compounds) were quantified by GC-MS/MS or LC-MS/MS in 85 bee bread samples and 154 pollen samples obtained from five apiaries each with three or four colonies (genotype Buckfast) in Luxembourg over the period 2011–2013. Thiacloprid, chlorfenvinphos, tebuconazole, and methiocarb were found most frequently in bee bread while thiacloprid, permethrin-cis, and permethrin-trans were detected most frequently in the pollen samples. Three neonicotinoid insecticides (clothianidin, imidacloprid, and thiamethoxam) that were restricted by an EU regulation in 2013 after our sampling campaign was finished were each found in less than 8% of the pollen or bee bread samples. The maximum concentrations of thiacloprid, metazachlor, and methiocarb measured in the pollen collected by a group of honeybee colonies (n = 5) without survivors within the 3-year period of observation were 86.20 ± 10.74 ng/g, 2.80 ± 1.26 ng/g, and below the limit of quantification, respectively. The maximum concentrations of the same compounds measured in the pollen collected by a group of honeybee colonies with significantly (P = 0.02) more survivors (7 out of 9) than expected, if the survivors had been distributed randomly among the groups of colonies, were 11.98 ± 2.28 ng/g, 0.44 ± 0.29 ng/g, and 8.49 ± 4.13 ng/g, respectively. No honeybee colony that gathered pollen containing more than 23 ng/g thiacloprid survived the 3-year project period. There was no statistically significant association between pesticide residues in the bee bread and the survival of the colonies. Actions already taken or planned and potential further actions to protect bees from exposure to pesticides are discussed.
KeywordsApis mellifera Crop protection Pollinator decline Food quality Varroa control
We thank Jean-Paul Beck and Roger Dammé (Fédération des Unions d’Apiculteurs du Grand-Duché de Luxembourg, FUAL) for organizational support, Jacques Engel and Andreas Reichart for helpful discussions, the “Administration des Services Techniques de l’Agriculture” in Luxembourg for the financial support of the “BeeFirst” project, the beekeepers of the FUAL honeybee breeding group for their invaluable support during the sampling campaigns, Léa Tison (INRA Centre de Recherche PACA, Unité “Abeilles et Environnement,” Avignon) for critical comments on an early version of the manuscript, and Lindsey Auguin for language editing.
Compliance with ethical standards
This article does not contain any studies with human subjects performed by any of the authors. The treatments of the animals reported in the manuscript comply with the local animal welfare laws, guidelines, and policies.
Conflict of interest
The authors declare that they have no conflict of interest.
- Anastassiades M, Lehotay SJ, Stajnbaher D, Schenck FJ (2003) Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. J AOAC Int 86:412–431Google Scholar
- Beyer M, Junk J, Eickermann M, Clermont A, Kraus F, Georges C, Reichart A, Hoffmann L (2018) Winter honey bee colony losses, Varroa destructor control strategies, and the role of weather conditions: results from a survey among beekeepers. Res Vet Sci 118C:52–60. https://doi.org/10.1016/j.rvsc.2018.01.012 CrossRefGoogle Scholar
- Bonmatin J-M, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, Marzaro M, Mitchell EAD, Noome DA, Simon-Delso N, Tapparo A (2015) Environmental fate and exposure; neonicotinoids and fipronil. Environ Sci Pollut Res 22:35–67. https://doi.org/10.1007/s11356-014-3332-7 CrossRefGoogle Scholar
- Bortolotti L, Montanari R, Marcelino J, Medrzycki P, Maini S, Porrini C (2003) Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull Insectology 56:63–68Google Scholar
- Chen M, Collins EM, Tao L, Lu C (2013) Simultaneous determination of residues in pollen and high-fructose corn syrup from eight neonicotinoid insecticides by liquid chromatography–tandem mass spectrometry. Anal Bioanal Chem 405(28):9251–9264. https://doi.org/10.1007/s00216-013-7338-7 CrossRefGoogle Scholar
- Clermont A, Eickermann M, Kraus F, Hoffmann L, Beyer M (2012) Untersuchungen zur Bienengesundheit in Luxemburg: Erste Ergebnisse aus den Jahren 2010 und 2011. 87th congress of German-speaking beekeepers, Echternach, Luxembourg, 13–16 September 2012. Book of Abstracts, page 17Google Scholar
- Daniele G, Giroud B, Jabot C, Vulliet E (2018) 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 25:6145–6153. https://doi.org/10.1007/s11356-017-9227-7 CrossRefGoogle Scholar
- de Miranda JR, Bailey L, Ball BV, Blanchard P, Budge GE, Chejanovsky N, Chen Y-P, Gauthier L, Genersch E, de Graaf DC, Ribière M, Ryabov E, De Smet L, van der Steen JJM (2013) Standard methods for virus research in Apis mellifera. J Apic Res 52:1–16. https://doi.org/10.3896/IBRA.220.127.116.11 CrossRefGoogle Scholar
- Doublet V, Labarussias M, de Miranda JR, Moritz RFA, Paxton RJ (2015) Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ Microbiol 17:969–983. https://doi.org/10.1111/1462-2920.12426 CrossRefGoogle Scholar
- European Commission (2013) Commission implementing Regulation (EU) No 485/2013 of 24 May 2013 amending Implementing Regulation (EU) No 540/2011, as regards the conditions of approval of the active substances clothianidin, thiamethoxam and imidacloprid, and prohibiting the use and sale of seeds treated with plant protection products containing those active substances. Off J Eur Union L139:12–26Google Scholar
- Giroud B, Vauchez A, Vulliet E, Wiest L, Buleté A (2013) Trace level determination of pyrethroid and neonicotinoid insecticides in beebread using acetonitrile-based extraction followed by analysis with ultra-high-performance liquid chromatography–tandem mass spectrometry. J Chromatogr A 1316:53–61. https://doi.org/10.1016/j.chroma.2013.09.088 CrossRefGoogle Scholar
- Heimbach U, Brandes M, Hausmann J, Ulber (2016) Effects of conventional and dropleg insecticide application techniques on pest during flowering of oilseed rape. IOBC/WPRS Bull 166:35–37Google Scholar
- Lehotay SJ, Maštovská K, Lightfield AR (2005) Use of buffering and other means to improve results of problematic pesticides in a fast and easy method for residue analysis of fruits and vegetables. J AOAC Int 88:615–629Google Scholar
- Pistorius J, Bischoff G, Heimbach U (2009) Bee poisoning by abrasion of active substances from seed treatment of maize during seeding in spring 2008. J Kulturpflanzen 61:9–14Google Scholar
- van der Zee R, Pisa L, Andonov S, Brodschneider R, Charrière J-D, Chlebo R, Coffey MF, Crailsheim K, Dahle B, Gajda A, Gray A, Drazic MM, Higes M, Kauko L, Kence A, Kence M, Kezic N, Kiprijanovska H, Kralj J, Kristiansen P, Hernandez RM, Mutinelli F, Nguyen BK, Otten C, Ozkirim A, Pernal SF, Peterson M, Ramsay G, Santrac V, Soroker V, Topolska G, Uzunov A, Vejsnaes F, Wei S, Wilkins S (2012) Managed honey bee colony losses in Canada, China, Europe, Israel and Turkey, for the winters of 2008–9 and 2009–10. J Apic Res 51:100–114. https://doi.org/10.3896/IBRA.18.104.22.168 CrossRefGoogle Scholar
- vanEngelsdorp D, Caron D, Hayes J, Underwood R, Henson KRM, Spleen A, Andree M, Snyder R, Lee K, Roccasecc K, Wilson M, Wilkes J, Lengerich R, Pettis J (2012) A national survey of managed honey bee 2010–11 winter colony losses in the USA: results from the Bee Informed Partnership. J Apic Res 51:115–124. https://doi.org/10.3896/IBRA.22.214.171.124 CrossRefGoogle Scholar