, Volume 27, Issue 5, pp 527–538 | Cite as

Sublethal effects of clothianidin and Nosema spp. on the longevity and foraging activity of free flying honey bees

  • Richard OdemerEmail author
  • Lisa Nilles
  • Nadine Linder
  • Peter Rosenkranz


Neonicotinoids alone or in combination with pathogens are considered to be involved in the worldwide weakening of honey bees. We here present a new approach for testing sublethal and/or synergistic effects in free flying colonies. In our experiment individually marked honey bees were kept in free flying mini-hives and chronically exposed to sublethal doses of the neonicotinoid clothianidin. Additional groups of bees were challenged with Nosema infections or with combinations of the pesticide and pathogens. Longevity and flight activity of the differentially treated bees were monitored for a period of 18 days. In contrast to previous laboratory studies, no effect of the neonicotinoid treatment on mortality or flight activity could be observed. Although the lifespan of Nosema infected bees were significantly reduced compared to non-infected bees a combination of pesticide and pathogen did not reveal any synergistic effect. Our results indicate that individual bees are less impaired by neonicotinoids if kept within the social environment of the colony. The effect of such a “social buffering” should be considered in future risk assessments.


Neonicotinoid clothianidin Honey bees Nosema Sublethal effects Field realistic Colony level 



We appreciate the support of the whole LAB staff for helping with the labelling of many individual bees. Emilia Semberg and Prof. Ingemar Fries from the SLU, Uppsala, performed the molecular identification of Nosema species with quantitative PCR analysis of Nosema samples. We also want to thank the reviewers for their valuable comments and suggestions that helped improving the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Alaux C, Brunet J-L, Dussaubat C, Mondet F, Tchamitchan S, Cousin M, Brillard J, Baldy A, Belzunces LP, Le Conte Y (2010) Interactions between Nosema microspores and a neonicotinoid weaken honey bees (Apis mellifera). Environ Microbiol 12:774–782. CrossRefGoogle Scholar
  2. Alkassab AT, Kirchner WH (2016) Impacts of chronic sublethal exposure to clothianidin on winter honey bees. Ecotoxicology 25:1000–1010. CrossRefGoogle Scholar
  3. Aufauvre J, Biron DG, Vidau C, Fontbonne R, Roudel M, Diogon M, Viguès B, Belzunces LP, Delbac F, Blot N (2012) Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honey bee. Sci Rep 2:1–7. CrossRefGoogle Scholar
  4. Blacquière T, Smagghe G, Van Gestel CAM, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–992. CrossRefGoogle Scholar
  5. 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 Insect 56:63–67Google Scholar
  6. Bryden J, Gill RJ, Mitton RAA, Raine NE, Jansen VAA (2013) Chronic sublethal stress causes bee colony failure. Ecol Lett 16:1463–1469. CrossRefGoogle Scholar
  7. Chaimanee V, Evans JD, Chen Y, Jackson C, Pettis JS (2016) Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos. J Insect Physiol 89:1–8. CrossRefGoogle Scholar
  8. Charreton M, Decourtye A, Henry M, Rodet G, Sandoz J-C, Charnet P, Collet C (2015) A locomotor deficit induced by sublethal doses of pyrethroid and neonicotinoid insecticides in the honey bee Apis mellifera. PLoS One 10:e0144879. CrossRefGoogle Scholar
  9. Chen Y, Evans JD, Smith IB, Pettis JS (2008) Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. J Invertebr Pathol 97:186–188. CrossRefGoogle Scholar
  10. Collison E, Hird H, Cresswell J, Tyler C (2016) Interactive effects of pesticide exposure and pathogen infection on bee health—a critical analysis. Biol Rev 44:1006–1019. CrossRefGoogle Scholar
  11. Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:149–157. CrossRefGoogle Scholar
  12. Cresswell JE, Thompson HM (2012) Comment on “A common pesticide decreases foraging success and survival in honey bees”. Science 337:1453. author reply 1453. CrossRefGoogle Scholar
  13. Cutler GC, Scott-Dupree CD (2007) Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. J Econ Entomol 100:765–772.[765:ETCSCH]2.0.CO;2 CrossRefGoogle Scholar
  14. Cutler GC, Scott-Dupree CD, Sultan M, McFarlane AD, Brewer L (2014) A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. PeerJ 2:e652. CrossRefGoogle Scholar
  15. Deutscher Wetterdienst DWD (2013) Deutschlandwetter im Juli 2013 Sonnig, warm und trocken - ein Sommermonat wie aus dem Bilderbuch. Pressemitteilung. Accessed 26 Jan 2014
  16. Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, Nazzi F, Gargiulo G, Pennacchio F (2013) Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc Natl Acad Sci 110:18466–18471. CrossRefGoogle Scholar
  17. 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. CrossRefGoogle Scholar
  18. Dussaubat C, Maisonnasse A, Crauser D, Beslay D, Costagliola G, Soubeyrand S, Kretzchmar A, Le Conte Y (2013) Flight behavior and pheromone changes associated to Nosema ceranae infection of honey bee workers (Apis mellifera) in field conditions. J Invertebr Pathol 113:42–51. CrossRefGoogle Scholar
  19. Dussaubat C, Maisonnasse A, Crauser D, Tchamitchian S (2016) Combined neonicotinoid pesticide and parasite stress alter honey bee queens’ physiology and survival. Sci Rep 6:314330. CrossRefGoogle Scholar
  20. EFSA (2012) EFSA Statement on the findings in recent studies investigating sub-lethal effects in bees of some neonicotinoids in consideration of the uses currently authorised in Europe. J Eur Union 10:1–27. CrossRefGoogle Scholar
  21. EFSA (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. J Eur Union L 139:12–26Google Scholar
  22. Elbert A, Haas M, Springer B, Thielert W, Nauen R (2008) Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 64:1099–1105. CrossRefGoogle Scholar
  23. Ellis C, Park KJ, Whitehorn P, David A, Goulson D (2017) The Neonicotinoid Insecticide thiacloprid impacts upon bumblebee colony development under field conditions. Environ Sci Technol 51:1727–1732. CrossRefGoogle Scholar
  24. Faucon JP, Aurières C, Drajnudel P, Mathieu L, Ribière M, Martel AC, Zeggane S, Chauzat MP, Aubert MFA (2005) Experimental study on the toxicity of imidacloprid given in syrup to honey bee (Apis mellifera) colonies. Pest Manag Sci 61:111–125. CrossRefGoogle Scholar
  25. Fischer J, Müller T, Spatz A-K, Greggers U, Grünewald B, Menzel R (2014) Neonicotinoids interfere with specific components of navigation in honey bees. PLoS One 9:e91364. CrossRefGoogle Scholar
  26. Fontbonne R, Garnery L, Vidau C, Aufauvre J, Texier C, Tchamitchian S, El Alaoui H, Brunet J-L, Delbac F, Biron DG (2013) Comparative susceptibility of three Western honeybee taxa to the microsporidian parasite Nosema ceranae. Infect Genet Evol 17:188–194. CrossRefGoogle Scholar
  27. Forsgren E, Fries I (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet Parasitol 170:212–217. CrossRefGoogle Scholar
  28. Fries I (2010) Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 103:S73–9. CrossRefGoogle Scholar
  29. Fries I, Lindström A, Rosenkranz P, Frey E, Odemer R, Schroeder A, de Miranda JR, Yañez O, Paxton RJ (2011) The principal parasites and pathogens of honeybees. In: Bees in Europe and sustainable honey production, Nova Science Publishers, Inc., New York, USA. pp 1–57Google Scholar
  30. Fries I, Chauzat M-P, Chen Y-P, Doublet V, Genersch E, Gisder S, Higes M, McMahon DP, Martín-Hernández R, Natsopoulou M, Paxton RJ, Tanner G, Webster TC, Williams GR (2013) Standard methods for Nosema research. J Apic Res 52:1–28. CrossRefGoogle Scholar
  31. Gallai N, Salles JM, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821. CrossRefGoogle Scholar
  32. Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97. CrossRefGoogle Scholar
  33. Genersch E, Von Der Ohe W, Kaatz H, Schroeder A, Otten C, Büchler R, Berg S, Ritter W, Mühlen W, Gisder S, Meixner M, Liebig G, Rosenkranz P (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332–352. CrossRefGoogle Scholar
  34. Girolami V, Mazzon L, Squartini A, Mori N, Marzaro M, Di Bernardo A, Greatti M, Giorio C, Tapparo A (2009) Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: a novel way of intoxication for bees. J Econ Entomol 102:1808–1815. CrossRefGoogle Scholar
  35. Gisder S, Hedtke K, Möckel N, Frielitz M-C, Linde A, Genersch E (2010) Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Appl Environ Microbiol 76:3032–8. CrossRefGoogle Scholar
  36. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science (80-) 347:1255957. CrossRefGoogle Scholar
  37. Goss J (2014) Neonicotinoids and honeybee health—The effect of the neonicotinoid clothianidin, applied as a seed dressing in Brassica napus, on pathogen and parasite prevalence and quantities in free-foraging adult honeybees (Apis mellifera). Master thesis, Swedish University of Agricultural SciencesGoogle Scholar
  38. Guez D (2013) A common pesticide decreases foraging success and survival in honey bees: questioning the ecological relevance. Front Physiol 4:2012–2014. CrossRefGoogle Scholar
  39. Henry M, Beguin 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 (80-) 336:348–350. CrossRefGoogle Scholar
  40. Henry M, Cerrutti N, Aupinel P, Decourtye A, Gayrard M, Odoux J-F, Pissard A, Rüger C, Bretagnolle V (2015) Reconciling laboratory and field assessments of neonicotinoid toxicity to honey bees. Proc R Soc B Biol Sci 282:20152110. CrossRefGoogle Scholar
  41. Higes M, Meana A, Bartolomé C, Botías C, Martín-Hernández R (2013) Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol Rep 5:17–29. CrossRefGoogle Scholar
  42. Holt HL, Aronstein KA, Grozinger CM (2013) Chronic parasitization by Nosema microsporidia causes global expression changes in core nutritional, metabolic and behavioral pathways in honey bee workers (Apis mellifera). BMC Genomics 14:799. CrossRefGoogle Scholar
  43. Huang Q, Kryger P, Le Conte Y, Moritz RFA (2012) Survival and immune response of drones of a Nosemosis tolerant honey bee strain towards N. ceranae infections. J Invertebr Pathol 109:297–302. CrossRefGoogle Scholar
  44. Huang Q, Kryger P, Le Conte Y, Lattorff HMG, Kraus FB, Moritz RFA (2013) Four quantitative trait loci associated with low Nosema ceranae (Microsporidia) spore load in the honeybee Apis mellifera. Apidologie 45(2):248–256. CrossRefGoogle Scholar
  45. Huang Q, Lattorff HMG, Kryger P, Le Conte Y, Moritz RFA (2014) A selective sweep in a microsporidian parasite Nosema-tolerant honeybee population, Apis mellifera. Anim Genet 45(2):267–273CrossRefGoogle Scholar
  46. Iwasa T, Motoyama N, Ambrose JT, Roe RM (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee. Apis mellifera Crop Prot 23:371–378. CrossRefGoogle Scholar
  47. Kairo G, Provost B, Tchamitchian S, Ben Abdelkader F, Bonnet M, Cousin M, Sénéchal J, Benet P, Kretzschmar A, Belzunces LP, Brunet J-L (2016) Drone exposure to the systemic insecticide Fipronil indirectly impairs queen reproductive potential. Sci Rep 6:31904. CrossRefGoogle Scholar
  48. Karahan A, Çakmak I, Hranitz JM, Karaca I, Wells H (2015) Sublethal imidacloprid effects on honey bee flower choices when foraging. Ecotoxicology 24:2017–2025. CrossRefGoogle Scholar
  49. Kessler SC, Tiedeken EJ, Simcock KL, Derveau S, Mitchell J, Softley S, Radcliffe A, Stout JC, Wright GA (2016) Corrigendum: Bees prefer foods containing neonicotinoid pesticides. Nature 533:278–278. CrossRefGoogle Scholar
  50. Lu C, Warchol KM, Callahan RA (2014) Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder. Bull Insect 67:125–130. ISSN 1721-8861Google Scholar
  51. Lundin O, Rundlöf M, Smith HG, Fries I, Bommarco R (2015) Neonicotinoid insecticides and their impacts on bees: a systematic review of research approaches and identification of knowledge gaps. PLoS One 10:e0136928. CrossRefGoogle Scholar
  52. Martín-Hernández R, Meana A, García-Palencia P, Marín P, Botías C, Garrido-Bailón E, Barrios L, Higes M (2009) Effect of temperature on the biotic potential of honey bee microsporidia. Appl Environ Microbiol 75:2554–7. CrossRefGoogle Scholar
  53. Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573–580. CrossRefGoogle Scholar
  54. Matsumoto T (2013) Reduction in homing flights in the honey bee Apis mellifera after a sublethal dose of neonicotinoid insecticides. Bull Insect 66:1–9Google Scholar
  55. Moritz RFA, Erler S (2016) Lost colonies found in a data mine: global honey trade but not pests or pesticides as a major cause of regional honey bee colony declines. Agric Ecosyst Environ 216:44–50. CrossRefGoogle Scholar
  56. Natsopoulou ME, McMahon DP, Doublet V, Bryden J, Paxton RJ (2014) Interspecific competition in honeybee intracellular gut parasites is asymmetric and favours the spread of an emerging infectious disease. Proc R Soc B Biol Sci 282:20141896–20141896. CrossRefGoogle Scholar
  57. Paxton R (2010) Does infection by Nosema ceranae cause “Colony Collapse Disorder” in honey bees (Apis mellifera)? J Apic Res 49:80. CrossRefGoogle Scholar
  58. Pecenka JR, Lundgren JG (2015) Non-target effects of clothianidin on monarch butterflies. Sci Nat 102:19. CrossRefGoogle Scholar
  59. Pettis JS, Lichtenberg EM, Andree M, Stitzinger J, Rose R, vanEngelsdorp D (2013) Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS One.
  60. Pettis JS, vanEngelsdorp D, Johnson J, Dively G (2012) Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99:153–158. CrossRefGoogle Scholar
  61. Pilling E, Campbell P, Coulson M, Ruddle N, Tornier I (2013) A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam. PLoS One 8:e77193. CrossRefGoogle Scholar
  62. Pistorius J, Bischoff G, Heimbach U, Stähler M (2010) Bee poisoning incidents in Germany in spring 2008 caused by abrasion of active substance from treated seeds during sowing of maize. Julius-Kühn-Archiv 423:118–126Google Scholar
  63. Pohorecka K, Skubida P, Miszczak A, Semkiw P, Sikorski P, Zagibajlo K, Teper D, Koltowski Z, Skubida M, Zdanska D, Bober A (2012) Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. J Apic Sci 56:115–134. CrossRefGoogle Scholar
  64. Pohorecka K, Skubida P, Semkiw P, Miszczak A, Teper D, Sikorski P, Zagibajlo K, Skubida M, Zdańska D, Bober A (2013) Effects of exposure of honey bee colonies to neonicotinoid seed-treated maize crops. J Apic Sci 57:199–208. CrossRefGoogle Scholar
  65. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: Trends, impacts and drivers. Trends Ecol Evol 25:345–353. CrossRefGoogle Scholar
  66. Reetz JE, Zühlke S, Spiteller M, Wallner K (2011) Neonicotinoid insecticides translocated in guttated droplets of seed-treated maize and wheat: a threat to honey bees? Apidologie 42:596–606. CrossRefGoogle Scholar
  67. Retschnig G, Williams GR, Odemer R, Boltin J, Di Poto C, Mehmann MM, Retschnig P, Winiger P, Rosenkranz P, Neumann P (2015) Effects, but no interactions, of ubiquitous pesticide and parasite stressors on honey bee (Apis mellifera) lifespan and behavior in a colony environment. Environ Microbiol 17:4322–4331. CrossRefGoogle Scholar
  68. Rolke D, Fuchs S, Grünewald B, Gao Z, Blenau W (2016) Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in Northern Germany: effects on honey bees (Apis mellifera). Ecotoxicology 25:1648–1665. CrossRefGoogle Scholar
  69. Rosenkranz P, von der Ohe W, Moritz RFA, Büchler R, Berg S, Otten C (2013) Schlussbericht Deutsches Bienenmonitoring—“DeBiMo”. Bundesanstalt für Landwirtschaft und Ernährung (BLE), Accessed 12 Nov 2017
  70. Rundlöf M, Andersson GKS, Bommarco R, Fries I, Hederström V, Herbertsson L, Jonsson O, Klatt BK, Pedersen TR, Yourstone J, Smith HG (2015) Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521:77–80. CrossRefGoogle Scholar
  71. Sánchez-Bayo F, Goulson D, Pennacchio F, Nazzi F, Goka K, Desneux N (2016) Are bee diseases linked to pesticides? A brief review. Environ Int 89–90:7–11. CrossRefGoogle Scholar
  72. Schmuck R, Schöning R, Stork A, Schramel O (2001) Risk posed to honey bees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 57:225–238. CrossRefGoogle Scholar
  73. Schneider CW, Tautz J, Grünewald B, Fuchs S (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS One 7:e30023. CrossRefGoogle Scholar
  74. Scholer J, Krischik V (2014) Chronic exposure of imidacloprid and clothianidin reduce queen survival, foraging, and nectar storing in colonies of bombus impatiens. PLoS One.
  75. 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 sub-lethal concentrations of the neonicotinoid insecticide thiacloprid. Pest Manag Sci.
  76. Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, Mcfield M, Mineau P, Mitchell EA, Morrissey CA, Noome DA, Pisa L, Settele J, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Van Der Sluijs JP, Whitehorn PR, Wiemers M (2015) Systemic insecticides (Neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environ Sci Pollut Res 22:5–34. CrossRefGoogle Scholar
  77. Smart MD, Sheppard WS (2012) Nosema ceranae in age cohorts of the western honey bee (Apis mellifera). J Invertebr Pathol 109:148–51. CrossRefGoogle Scholar
  78. Sponsler DB, Johnson RM (2017) Mechanistic modeling of pesticide exposure: the missing keystone of honey bee toxicology. Environ Toxicol Chem 36:871–881. CrossRefGoogle Scholar
  79. Stankus T (2014) Reviews of science for science librarians: an update on honeybee colony collapse disorder. Sci Technol Libr 33:228–260. CrossRefGoogle Scholar
  80. Staveley JP, Law SA, Fairbrother A, Menzie CA (2014) A causal analysis of observed declines in managed honey bees (Apis mellifera). Hum Ecol Risk Assess Int J 20:566–591. CrossRefGoogle Scholar
  81. Straub L, Williams GR, Pettis J, Fries I, Neumann P (2015) Superorganism resilience: eusociality and susceptibility of ecosystem service providing insects to stressors. Curr Opin Insect Sci 12:109–112. CrossRefGoogle Scholar
  82. Thompson H, Coulson M, Ruddle N, Wilkins S, Harkin S (2016) Thiamethoxam: assessing flight activity of honey bees foraging on treated oilseed rape using radio frequency identification technology. Environ Toxicol Chem 35:385–393. CrossRefGoogle Scholar
  83. Tosi S, Burgio G, Nieh JC (2017) A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Sci Rep 7:1201. CrossRefGoogle Scholar
  84. Tsvetkov N, Samson-Robert O, Sood K, Patel HS, Malena DA, Gajiwala PH, Maciukiewicz P, Fournier V, Zayed A (2017) Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science 356:1395–1397. CrossRefGoogle Scholar
  85. Van der Sluijs JP, Simon-Delso N, Goulson D, Maxim L, Bonmatin JM, Belzunces LP (2013) Neonicotinoids, bee disorders and the sustainability of pollinator services. Curr Opin Environ Sustain 5:293–305. CrossRefGoogle Scholar
  86. Vidau C, Diogon M, Aufauvre J, Fontbonne R, Viguès B, Brunet JL, Texier C, Biron DG, Blot N, Alaoui H, Belzunces LP, Delbac F (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honey bees previously infected by Nosema ceranae. PLoS One 6:e21550. CrossRefGoogle Scholar
  87. Williams GR, Troxler A, Retschnig G, Roth K, Yañez O, Shutler D, Neumann P, Gauthier L (2015) Neonicotinoid pesticides severely affect honey bee queens. Sci Rep 5:14621. CrossRefGoogle Scholar
  88. Williamson SM, Willis SJ, Wright GA (2014) Exposure to neonicotinoids influences the motor function of adult worker honey bees. Ecotoxicology 23:1409–1418. CrossRefGoogle Scholar
  89. Woodcock BA, Bullock JM, Shore RF, Heard MS, Pereira MG, Redhead J, Ridding L, Dean H, Sleep D, Henrys P, Peyton J, Hulmes S, Hulmes L, Sárospataki M, Saure C, Edwards M, Genersch E, Knäbe S, Pywell RF (2017) Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science (80-) 356:1393–1395. CrossRefGoogle Scholar
  90. Würfel T (2008) Abschlussbericht Beizung und Bienenschäden. Minist für Ernährung und ländlichen Raum 1–40., Accessed 18 Dec 2013
  91. Yang EC, Chuang YC, Chen YL, Chang LH (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 101:1743–1748. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Apicultural State InstituteUniversity of HohenheimStuttgartGermany

Personalised recommendations