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Environmental Science and Pollution Research

, Volume 25, Issue 32, pp 32163–32177 | Cite as

Pesticide residue profiles in bee bread and pollen samples and the survival of honeybee colonies—a case study from Luxembourg

  • Marco Beyer
  • Audrey Lenouvel
  • Cédric Guignard
  • Michael Eickermann
  • Antoine Clermont
  • François Kraus
  • Lucien Hoffmann
Research Article

Abstract

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.

Keywords

Apis mellifera Crop protection Pollinator decline Food quality Varroa control 

Notes

Acknowledgements

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.

References

  1. 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
  2. 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
  3. 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
  4. 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
  5. Brandt A, Gorenflo A, Siede R, Meixner M, Büchler R (2016) The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). J Insect Physiol 86:40–47.  https://doi.org/10.1016/j.jinsphys.2016.01.001 CrossRefGoogle Scholar
  6. Brodschneider R, Craisheim K (2000) Nutrition and health in honey bees. Apidologie 41:278–294.  https://doi.org/10.1051/apido/2010012 CrossRefGoogle Scholar
  7. 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
  8. 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
  9. Clermont A, Eickermann M, Kraus F, Georges C, Hoffmann L, Beyer M (2014) A survey on some factors potentially affecting losses of managed honey bee colonies in Luxembourg over the winters 2010/2011 and 2011/2012. J Apic Res 53:43–56.  https://doi.org/10.3896/IBRA.1.53.1.04 CrossRefGoogle Scholar
  10. Clermont A, Eickermann M, Kraus F, Hoffmann L, Beyer M (2015a) Correlations between land covers and honey bee colony losses in a country with industrialized and rural regions. Sci Total Environ 562:1–13.  https://doi.org/10.1016/j.scitotenv.2015.05.128 CrossRefGoogle Scholar
  11. Clermont A, Pasquali M, Eickermann M, Kraus F, Hoffmann L, Beyer M (2015b) Virus status, varroa levels and survival of 20 managed honey bee colonies monitored in Luxembourg between summer 2011 and spring 2013. J Apic Sci 59:59–73.  https://doi.org/10.1515/jas-2015-0005 CrossRefGoogle Scholar
  12. Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P (2012) Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. App Environ Microbiol 78:981–987.  https://doi.org/10.1128/AEM.06537-11 CrossRefGoogle Scholar
  13. 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
  14. 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.1.52.4.22 CrossRefGoogle Scholar
  15. 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
  16. Ellis AM, Hayes GW Jr (2009) An evaluation of fresh versus fermented diets for honey bees (Apis mellifera). J Apic Res 48:215–216.  https://doi.org/10.3896/IBRA.1.48.3.11 CrossRefGoogle Scholar
  17. 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
  18. Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821.  https://doi.org/10.1016/j.ecolecon.2008.06.014 CrossRefGoogle Scholar
  19. 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
  20. 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
  21. Karier P, Kraus G, Kolber I (2017) Metazachlor traces in the main drinking water reservoir in Luxembourg: a scientific and political discussion. Environ Sci Eur 29(25):25.  https://doi.org/10.1186/s12302-017-0123-z CrossRefGoogle Scholar
  22. Korta E, Bakkali A, Berrueta LA, Gallo B, Vicente F, Bogdanov S (2003) Determination of amitraz and other acaricide residues in beeswax. Anal Chim Acta 475:97–103.  https://doi.org/10.1016/S0003-2670(02)01221-7 CrossRefGoogle Scholar
  23. 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
  24. Mõtus K, Raie A, Orro T, Chauzat M-P, Viltrop A (2016) Epidemiology, risk factors and varroa mite control in the Estonian honey bee population. J Apic Res 55:396–412.  https://doi.org/10.1080/00218839.2016.1251081 CrossRefGoogle Scholar
  25. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, vanEngelsdorp D, Pettis JS (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One 5:e9754.  https://doi.org/10.1371/journal.pone.0009754 CrossRefGoogle Scholar
  26. Naug D (2009) Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol Conserv 142:2369–2372.  https://doi.org/10.1016/j.biocon.2009.04.007 CrossRefGoogle Scholar
  27. 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
  28. Sanchez-Bayo F, Goka K (2014) Pesticide residues and bees – a risk assessment. PLoS One 9(4):e94482.  https://doi.org/10.1371/journal.pone.0094482 CrossRefGoogle Scholar
  29. Sandrock C, Tanadini M, Tanadini LG, Fauser-Misslin A, Potts SG, Neumann P (2014) Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure. PLoS One 9(8):e103592.  https://doi.org/10.1371/journal.pone.0103592 CrossRefGoogle Scholar
  30. Siede R, Faust L, Meixner MD, Maus C, Grünewald B, Büchler R (2017) Performance of honey bee colonies under a long-lasting dietary exposure to sublethal concentrations of the neonicotinoid insecticide thiacloprid. Pest Manag Sci 73:1334–1344.  https://doi.org/10.1002/ps.4547 CrossRefGoogle Scholar
  31. Switanek M, Crailsheim K, Truhetz H, Brodschneider R (2017) Modelling seasonal effects of temperature and precipitation on honey bee winter mortality in a temperate climate. Sci Total Environ 579:1581–1587.  https://doi.org/10.1016/j.scitotenv.2016.11.178 CrossRefGoogle Scholar
  32. Thomas MR (2001) Pesticide usage monitoring in the United Kingdom. Ann Occup Hyg 45:S87–S93CrossRefGoogle Scholar
  33. Thompson HE, Fryday SL, Harkin S, Milner S (2014) Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops. Apidologie 45:545–553.  https://doi.org/10.1007/s13592-014-0273-6 CrossRefGoogle Scholar
  34. Tison L, Hahn ML, Holtz S, Rößner A, Greggers U, Bischoff G, Menzel R (2016) Honey bees’ behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field. Environ Sci Technol 50:7218–7227.  https://doi.org/10.1021/acs.est.6b02658 CrossRefGoogle Scholar
  35. 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.1.51.1.12 CrossRefGoogle Scholar
  36. 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.1.51.1.12 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Environmental Research and Innovation DepartmentLuxembourg Institute of Science and TechnologyBelvauxLuxembourg
  2. 2.IRSTEA MontpellierMontpellierFrance
  3. 3.Administration des Services Techniques de l’AgricultureLuxembourgLuxembourg

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