Skip to main content
SpringerLink
Log in

Sublethal exposure to neonicotinoids and related side effects on insect pollinators: honeybees, bumblebees, and solitary bees

  • Review
  • Published:
Journal of Plant Diseases and Protection Aims and scope Submit manuscript

Abstract

Nowadays, there are increasing concerns about the bioavailability of neonicotinoids in the environment and possible exposure of nontarget organisms to these insecticides, their residues having been detected at different concentrations in many matrices, i.e., pollen, nectar, soil, water. Regarding the risk assessment process, there are still some information gaps about the exposure pathways and the possibility of various sublethal effects on insect pollinators. Recently, a clear rapprochement between the sublethal effects of different endpoints under laboratory conditions and field-realistic exposure level has been demonstrated. Here, we attempt to draw general portrayal about the current debate of the exposure to neonicotinoids and their impacts on pollinators. Depending on our extracted data from the published literature, we show that the lowest observed effect concentration under realistic field conditions in the most cases is higher than under laboratory conditions, which indicate that further long-term field research is required with consideration that our good understanding of the pollinators’ responses to sublethal exposure should be taken into account in the future experimental design in order to establish vigorous conclusions. We review currently available information in the published literature, presenting the reports about detected residues in relation to multiple ways of exposure and their potential consequences on insect pollinators and community dynamics. Nevertheless, we attempt to classify the sublethal effects depending on the different biological levels from genes to population. Moreover, we consider the field-realistic exposure level and critically analyze the laboratory as well as field studies to specify their physiological and behavioral effects. Additionally, synergistic effects of different factors, including exposure to neonicotinoids and their hazards on bees, will find special attention.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Abbo PM, Kawasaki JK, Hamilton M, Cook SC, DeGrandi-Hoffman G, Li WF, Liu J, Chen YP (2016) Effects of imidacloprid and Varroa destructor on survival and health of European honey bees, Apis mellifera. Insect Sci. doi:10.1111/1744-7917.12335

    PubMed  Google Scholar 

  2. Abbott VA, Nadeau JL, Higo HA, Winston ML (2008) Lethal and sublethal effects of imidacloprid on Osmia lignaria and clothianidin on Megachile rotundata (Hymenoptera: Megachilidae). J Econ Entomol 101:784–796

    Article  CAS  PubMed  Google Scholar 

  3. Alaux C, Brunet JL, 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 honeybees (Apis mellifera). Environ Microbiol 12:774–782

    Article  PubMed  PubMed Central  Google Scholar 

  4. Aliouane Y, El Hassani AK, Gary V, Armengaud C, Lambin M, Gauthier M (2009) Sub-chronic exposure of honeybees to sublethal doses of pesticides: effects on behavior. Environ Toxicol Chem 28:113–122

    Article  CAS  PubMed  Google Scholar 

  5. Alkassab AT, Kirchner WH (2016) Impacts of chronic sublethal exposure to clothianidin on winter honeybees. Ecotoxicology 25:1000–1010

    Article  CAS  PubMed  Google Scholar 

  6. Alptekin S, Bass C, Nicholls C, Paine MJI, Clark SJ, Field L, Moores GD (2016) Induced thiacloprid insensitivity in honeybees (Apis mellifera L.) is associated with up-regulation of detoxification genes. Insect Mol Biol 25:171–180

    Article  CAS  PubMed  Google Scholar 

  7. APENET (2010) Effects of coated maize seed on honey bees. Report based on results obtained from the second year of activity of the ApeNet project. CRA-API, Bologna, Italy. http://www.reterurale.it/downloads/APENET_2010_Report_EN%206_11.pdf

  8. Aufauvre J, Misme-Aucouturier B, Vigues B, Texier C, Delbac F, Blot N (2014) Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLoS One 9:e91686

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Aumeier P (2001) Bioassay for grooming effectiveness towards Varroa destructor mites in Africanized and Carniolan honey bees. Apidologie 32:81–90

    Article  Google Scholar 

  10. Badawy MEI, Nasr HM, Rabea EI (2015) Toxicity and biochemical changes in the honey bee Apis mellifera exposed to four insecticides under laboratory conditions. Apidologie 46:177–193

    Article  CAS  Google Scholar 

  11. Badiou-Bénéteau A, Carvalho SM, Brunet JL, Carvalho GA, Buleté A et al (2012) Development of biomarkers of exposure to xenobiotics in the honey bee Apis mellifera: application to the systemic insecticide thiamethoxam. Ecotoxicol Environ Saf 82:22–31

    Article  PubMed  CAS  Google Scholar 

  12. Bodereau-Dubois B, List O, Calas-List D, Marques O, Communal PY, Thany SH, Lapied B (2012) Transmembrane potential polarization, calcium influx, and receptor conformational state modulate the sensitivity of the imidacloprid-insensitive neuronal insect nicotinic acetylcholine receptor to neonicotinoid insecticides. J Pharm Exp Ther 341:326–339

    Article  CAS  Google Scholar 

  13. Boily M, Sarrasin B, Deblois C, Aras P, Chagnon M (2013) Acetylcholinesterase in honey bees (Apis mellifera) exposed to neonicotinoids, atrazine and glyphosate: laboratory and field experiments. Environ Sci Pollut Res 8:5603–5614

    Article  CAS  Google Scholar 

  14. 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 Insectol 56:63–67

    Google Scholar 

  15. 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

    Article  CAS  PubMed  Google Scholar 

  16. Brown LA, Ihara M, Buckingham SD, Matsuda K, Sattelle DB (2006) Neonicotinoid insecticides display partial and super agonist actions on native insect nicotinic acetylcholine receptors. J Neurochem 99:608–615

    Article  CAS  PubMed  Google Scholar 

  17. Byrne FJ, Visscher PK, Leimkuehler B, Fischer D, Grafton-Cardwell EE et al (2014) Determination of exposure levels of honey bees foraging on flowers of mature citrus trees previously treated with imidacloprid. Pest Manag Sci 70:470–482

    Article  CAS  PubMed  Google Scholar 

  18. Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99–117

    Article  CAS  PubMed  Google Scholar 

  19. Catae AF, Roat TC, De Oliveira RA, Nocelli RCF, Malaspina O (2014) Cytotoxic effects of thiamethoxam in the midgut and malpighian tubules of Africanized Apis mellifera (Hymenoptera: Apidae). Microsc Res Tech 77:274–281

    Article  CAS  PubMed  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. Chauzat MP, Martel AC, Cougoule N, Porta P, Lachaize J, Zeggane S, Aubert M, Carpentier P, Faucon JP (2011) An assessment of honeybee colony matrices, Apis mellifera (Hymenoptera Apidae) to monitor pesticide presences in continental France. Environ Toxicol Chem 30:103–111

    Article  CAS  PubMed  Google Scholar 

  22. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA et al (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol 15:615–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Colin ME, Bonmatin JM, Moineau I, Gaimon C, Brun S, Vermandere JP (2004) A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticides. Arch Environ Contam Toxicol 47:387–395

    Article  CAS  PubMed  Google Scholar 

  24. Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:149–157

    Article  CAS  PubMed  Google Scholar 

  25. Cutler GC, Scott-Dupree CD (2014) A field study examining the effects of exposure to neonicotinoid seed-treated corn on commercial bumble bee colonies. Ecotoxicology 23:1755–1763

    Article  CAS  Google Scholar 

  26. 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

    Article  CAS  PubMed  Google Scholar 

  27. 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

    Article  PubMed  PubMed Central  Google Scholar 

  28. de Almeida Rossi C, Roat TC, Tavares DA, Cintra-Socolowski P, Malaspina O (2013) Effects of sublethal doses of imidacloprid in malpighian tubules of africanized Apis mellifera (Hymenoptera, Apidae). Microsc Res Tech 76:552–558

    Article  CAS  Google Scholar 

  29. de Almeida Rossi C, Roat TC, Tavares DA, Cintra-Socolowski P, Malaspina O (2013) Brain morphophysiology of Africanized bee Apis mellifera exposed to sublethal doses of imidacloprid. Arch Environ Contam Toxicol 65:234–243

    Article  PubMed  CAS  Google Scholar 

  30. Dechaume-Moncharmont FX, Decourtye A, Hennequet-Hantier C, Pons O, Pham-Delégue MH (2003) Statistical analysis of the honeybee survival after chronic exposure to insecticides. Environ Toxicol Chem 22:3088–3094

    Article  PubMed  Google Scholar 

  31. Decourtye A, Armengaud C, Renou M, Devillers J, Cluzeau S, Gauthier M, Pham-Delegue MH (2004) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pestic Biochem Phys 78:83–92

    Article  CAS  Google Scholar 

  32. Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delegue MH (2004) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57:410–419

    Article  CAS  PubMed  Google Scholar 

  33. Decourtye A, Devillers J, Genecque E, Le Menach K, Budzinski H, Cluzeau S, Pham-Delegue MH (2005) Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch Environ Contam Toxicol 48:242–250

    Article  CAS  PubMed  Google Scholar 

  34. Decourtye A, Lacassie E, Pham-Delegue MH (2003) Learning performances of honeybees (Apis mellifera L.) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59:269–278

    Article  CAS  PubMed  Google Scholar 

  35. Derecka K, Blythe MJ, Malla S, Genereux DP, Guffanti A, Pavan P et al (2013) Transient exposure to low levels of insecticide affects metabolic networks of honeybee larvae. PLoS One 8:e68191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  PubMed  Google Scholar 

  37. 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 USA 110:18466–18471

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Dively GP, Embrey MS, Kamel A, Hawthorne DJ, Pettis JS (2015) Assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLoS One 10:e0118748

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Doublet V, Labarussias M, Miranda JR, Moritz RF, 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

    Article  CAS  PubMed  Google Scholar 

  40. Dupuis J, Louis T, Gauthier M, Raymond V (2012) Insights from honeybee (Apis mellifera) and fly (Drosophila melanogaster) nicotinic acetylcholine receptors: from genes to behavioral functions. Neurosci Biobehav Rev 36:1553–1564

    Article  CAS  PubMed  Google Scholar 

  41. EFSA (European Food Safety Authority) (2012) 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. EFSA J 10:2752

    Article  CAS  Google Scholar 

  42. Eiri DM, Nieh JC (2012) A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. J Exp Biol 215:2022–2029

    Article  CAS  PubMed  Google Scholar 

  43. El Hassani AK, Dacher M, Gary V, Lambin M, Gauthier M, Armengaud C (2008) Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Arch Environ Contam Toxicol 54:653–661

    Article  PubMed  CAS  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

  45. Elston C, Thompson HM, Walters KF (2013) Sub-lethal effects of thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (Bombus terrestris) micro-colonies. Apidologie 44:563–57456

    Article  CAS  Google Scholar 

  46. European Commission (2013) European Commission, 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 139:12–26. http://eur-lex.europa.eu/legal-content/EN/ALL/?uri=CELEX:32013R0485

  47. Faucon JP, Auriéres C, Drajnudel P, Mathieu L, Ribiére 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

    Article  CAS  PubMed  Google Scholar 

  48. Fauser-Misslin A, Sadd BM, Neumann P, Sandrock C (2014) Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory. J Appl Ecol 51:450–459

    Article  Google Scholar 

  49. Feltham H, Park K, Goulson D (2014) Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23:317–323

    Article  CAS  PubMed  Google Scholar 

  50. Fischer J, Müller T, Spatz AK, Greggers U, Grünewald B, Menzel R (2014) Neonicotinoids interfere with specific components of navigation in honeybees. PLoS One 9:e91364

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Franklin MT, Winston ML, Morandin LA (2004) Effects of clothianidin on Bombus impatiens (Hymenoptera: Apidae) colony health and foraging ability. J Econ Entomol 97:369–373

    Article  CAS  PubMed  Google Scholar 

  52. Gawleta N, Zimmermann Y, Eltz T (2005) Repellent foraging scent recognition across bee families. Apidologie 36:325–335

    Article  Google Scholar 

  53. Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C, Büchler R et al (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332–352

    Article  CAS  Google Scholar 

  54. Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Girolami V, Mazzon L, Squartini A, Mori N, Marzaro M, Dibernardo A, Greatti M, Giorio C, Tapparos 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

    Article  CAS  PubMed  Google Scholar 

  56. Giurfa M (1993) The repellent scent-mark of the honeybee Apis mellifera ligustica and its role as communication cue during foraging. Insect Soc 40:59–67

    Article  Google Scholar 

  57. Gregorc A, Ellis JD (2011) Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pest Biochem Physiol 99:200–207

    Article  CAS  Google Scholar 

  58. Gregorc A, Evans JD, Scharf M, Ellis JD (2012) Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor). J Insect Physiol 58:1042–1049

    Article  CAS  PubMed  Google Scholar 

  59. Gregorc A, Silva-Zacarin EC, Carvalho SM, Kramberger D, Teixeira EW, Malaspina O (2016) Effects of Nosema ceranae and thiametoxam in Apis mellifera: a comparative study in Africanized and Carniolan honey bees. Chemosphere 147:328–336

    Article  CAS  PubMed  Google Scholar 

  60. Guez D, Belzunces LP, Maleszka R (2003) Effects of imidacloprid metabolites on habituation in honeybees suggest the existence of two subtypes of nicotinic receptors differentially expressed during adult development. Pharmacol Biochem Behav 75:217–222

    Article  CAS  PubMed  Google Scholar 

  61. Guez D, Suchail S, Gauthier M, Maleszka R, Belzunces LP (2001) Contrasting effects of imidacloprid on habituation in 7- and 8-day-old honeybees (Apis mellifera). Neurobiol Learn Mem 76:183–191

    Article  CAS  PubMed  Google Scholar 

  62. Haith DA (2010) Ecological risk assessment of pesticide runoff from grass surfaces. Environ Sci Technol 44:6496–6502

    Article  CAS  PubMed  Google Scholar 

  63. Han P, Niu CY, Lei CL, Cui JJ, Desneux N (2010) Use of an innovative T-tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera L. Ecotoxicology 19:1612–1619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hatjina F, Papaefthimiou C, Charistos L, Dogaroglu T, Bouga M et al (2013) Sublethal doses of imidacloprid decreased size of hypopharyngeal glands and respiratory rhythm of honeybees in vivo. Apidologie 44:467–480

    Article  CAS  Google Scholar 

  65. Henry M, Beguin M, Requier F, Rollin O, Odoux JF, Aupinel P, Aptel J, Tchamitchian S, Decourtye A (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336:348–350

    Article  CAS  PubMed  Google Scholar 

  66. Heylen K, Gobin B, Arckens L, Huybrechts R, Billen J (2011) The effects of four crop protection products on the morphology and ultrastructure of the hypopharyngeal gland of the European honeybee, Apis mellifera. Apidologie 42:103–116

    Article  CAS  Google Scholar 

  67. Iwasa T, Motoyama N, Ambrose JT, Roe MR (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot 23:371–378

    Article  CAS  Google Scholar 

  68. Jeschke P, Nauen R (2008) Neonicotinoids-from zero to hero in insecticide chemistry. Pest Manag Sci 64:1084–1098

    Article  CAS  PubMed  Google Scholar 

  69. Joachimsmeier I, Pistorius J, Schenke D, Kirchner WH (2012) Guttation and risk for honeybee colonies (Apis mellifera L.): use of guttation drops by honey bees after migration of colonies—a field study. Jul Kuhn. doi:10.5073/jka.2012.437.016

    Google Scholar 

  70. Jones A, Harrington P, Turnbull G (2014) Neonicotinoid concentrations in arable soils after seed treatment applications in preceding years. Pest Manag Sci 70:1780–1784

    Article  CAS  PubMed  Google Scholar 

  71. Kessler SC, Tiedeken EJ, Simcock KL, Derveau S, Mitchell J, Softley S et al (2015) Bees prefer foods containing neonicotinoid pesticides. Nature 521:74–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Kirchner WH (1999) Mad-bee-disease? Sublethal effects of imidacloprid (Gaucho) on the behaviour of honeybees. Apidologie 30:421–422

    Article  Google Scholar 

  73. Klein AM, Vaissiére BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc Biol Sci 274:303–313

    Article  PubMed  Google Scholar 

  74. Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One 7:e29268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lambin M, Armengaud C, Raymond S, Gauthier M (2001) Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. Arch Insect Biochem Physiol 48:129–134

    Article  CAS  PubMed  Google Scholar 

  76. Larson JL, Redmond CT, Potter DA (2013) Assessing insecticide hazard to bumble bees foraging on flowering weeds in treated lawns. PLoS One 8:e66375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Lawrence TJ, Culbert EM, Felsot AS, Hebert VR, Sheppard WS (2016) Survey and risk assessment of Apis mellifera (Hymenoptera: Apidae) exposure to neonicotinoid pesticides in urban, rural, and agricultural settings. J Econ Entomol 109:520–528

    Article  CAS  PubMed  Google Scholar 

  78. Laycock I, Cotterell KC, O’Shea-Wheller TA, Cresswell JE (2014) Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on microcolonies of Bombus terrestris worker bumble bees. Ecotoxicol Environ Saf 100:153–158

    Article  CAS  PubMed  Google Scholar 

  79. Laycock I, Cresswell JE (2013) Repression and recuperation of brood production in Bombus terrestris bumble bees exposed to a pulse of the neonicotinoid pesticide imidacloprid. PLoS One 8:e79872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Laycock I, Lenthall KM, Barratt AT, Cresswell JE (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21:1937–1945

    Article  CAS  PubMed  Google Scholar 

  81. Lu C, Warchol KM, Callahan RA (2012) In situ replication of honey bee colony collapse disorder. Bull Insectol 65:99–106

    Google Scholar 

  82. Maisonnasse A, Lenoir JC, Beslay D, Crauser D, Le Conte Y (2010) E-β-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera). PLoS One 5:e13531

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Matsumoto T (2013) Reduction in homing flights in the honey bee Apis mellifera after a sublethal dose of neonicotinoid insecticides. Bull Insectol 66:1–9

    Google Scholar 

  84. Medrzycki P, Montanari R, Bortolotti L, Sabatini AG, Maini S, Porrini C (2003) Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests. Bull Insectol 56:59–62

    Google Scholar 

  85. Menzel R, De Marco RJ, Greggers U (2006) Spatial memory, navigation and dance behaviour in Apis mellifera. J Comp Physiol A 192:889–903

    Article  Google Scholar 

  86. Menzel R, Greggers U, Hammer M (1993) Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In: Papaj DR, Lewis AC (eds) Insect learning. Chapman Hall, New York, pp 79–125

    Chapter  Google Scholar 

  87. Moffat C, Pacheco JG, Sharp S, Samson AJ, Bollan KA, Huang J et al (2015) Chronic exposure to neonicotinoids increases neuronal vulnerability to mitochondrial dysfunction in the bumblebee (Bombus terrestris). FASEB J 29:2112–2119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Mommaerts V, Reynders S, Boulet J, Besard L, Sterk G, Smagghe G (2010) Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19:207–215

    Article  CAS  PubMed  Google Scholar 

  89. Morandin LA, Winston ML (2003) Effects of novel pesticides on bumble bee (Hymenoptera: Apidae) colony health and foraging ability. Environ Entomol 32:555–563

    Article  CAS  Google Scholar 

  90. 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 honeybee health. PLoS One 5:e9754

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Nikolakis A, Chapple A, Friessleben R, Neumann P, Schad T, Schmuck R et al (2009) An effective risk management approach to prevent bee damage due to the emission of abraded seed treatment particles during sowing of seeds treated with bee toxic insecticides. Jul Kühn Arch 423:132–148

    Google Scholar 

  92. Oliveira RA, Roat TC, Carvalho SM, Malaspina O (2014) Side-effects of thiamethoxam on the brain and midgut of the africanized honeybee Apis mellifera (Hymenopptera: Apidae). Environ Toxicol 29:1122–1133

    Article  CAS  PubMed  Google Scholar 

  93. Osborne JL (2012) Bumblebees and pesticides. Nature 491:43–45

    Article  CAS  PubMed  Google Scholar 

  94. Palmer MJ, Moffat C, Saranzewa N, Harvey J, Wright GA et al (2013) Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nat Commun 4:1634

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Pareja L, Colazzo M, Pérez-Parada A, Niell S, Carrasco-Letelier L, Besil N, Cesio MV et al (2011) Detection of pesticides in active and depopulated beehives in Uruguay. Int J Environ Res Public Health 8:3844–3858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Peng YC, Yang EC (2016) Sublethal dosage of imidacloprid reduces the microglomerular density of honey bee mushroom bodies. Sci Rep 6:19298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Peng YS, Fang Y, Xu S, Ge L (1987) The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite, Varroa jacobsoni Oudemans. J Invertebr Pathol 49:54–60

    Article  Google Scholar 

  98. 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 8:e70182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Piiroinen S, Botías C, Nicholls E, Goulson D (2016) No effect of low-level chronic neonicotinoid exposure on bumblebee learning and fecundity. PeerJ 4:e1808

    Article  PubMed  PubMed Central  Google Scholar 

  101. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Pohorecka K, Skubida P, Miszczak A, Semkiw P, Sikorski P, Zagibajlo K et al (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

    Google Scholar 

  103. Ramirez-Romero R, Chaufaux J, Pham-Delegue MH (2005) Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie 36:601–611

    Article  CAS  Google Scholar 

  104. Reetz JE, Schulz W, Seitz W, Spiteller M, Zühlke S, Armbruster W, Wallner K (2016) Uptake of neonicotinoid insecticides by water-foraging honey bees (Hymenoptera: Apidae) through guttation fluid of winter oilseed rape. J Econ Entomol 109:31–40

    Article  CAS  PubMed  Google Scholar 

  105. Retschnig G, Neumann P, Williams GR (2014) Thiacloprid-Nosema ceranae interactions in honey bees: host survivorship but not parasite reproduction is dependent on pesticide dose. J Invertebr Pathol 118:18–19

    Article  PubMed  Google Scholar 

  106. Retschnig G, Williams GR, Odemer R, Boltin J, Di Poto C, Mehmann MM et al (2015) Effects, but no interactions, of ubiquitous pesticide and parasite stressors on honey bee (Apis mellifera) lifespan and behaviour in a colony environment. Environ Microbiol 17:4322–4331

    Article  CAS  PubMed  Google Scholar 

  107. Rexrode M, Barrett M, Ellis J, Gabe P, Vaughan A, Felkel J, Melendez J (2003) EFED risk assessment for the seed treatment of clothianidin on corn and Canola. United States Environmental Protection Agency, Washington, DC

    Google Scholar 

  108. Rondeau G, Sánchez-Bayo F, Tennekes HA, Decourtye A, Ramírez-Romero R, Desneux N (2014) Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci Rep 4:5566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Rössler W, Groh C (2012) Plasticity of synaptic microcircuits in the mushroom-body calyx of the honey bee. In: Eisenhardt D, Giurfa M, Galizia CG (eds) Honeybee neurobiology and behavior—a tribute to Randolf Menzel. Springer, Dordrecht, pp 141–153

    Chapter  Google Scholar 

  110. Rundlöf M, Andersson GKS, Bommarco R, Fries I, Hederström V, Herbertsson L et al (2015) Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521:77–80

    Article  PubMed  CAS  Google Scholar 

  111. Samson-Robert O, Labrie G, Chagnon M, Fournier V (2014) Neonicotinoid-contaminated puddles of water represent a risk of intoxication for honey bees. PLoS One 9:e108443

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Samson-Robert O, Labrie G, Mercier PL, Chagnon M, Derome N, Fournier V (2015) Increased acetylcholinesterase expression in bumble bees during neonicotinoid-coated corn sowing. Sci Rep 5:12636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Sánchez-Bayo F, Hyne RV (2014) Detection and analysis of neonicotinoids in river waters-development of a passive sampler for three commonly used insecticides. Chemosphere 99:143–151

    Article  PubMed  CAS  Google Scholar 

  114. 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

    Article  PubMed  CAS  Google Scholar 

  115. Sandrock C, Tanadini LG, Pettis J, Biesmeijer JC, Potts SG et al (2014) Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agric For Entomol 16:119–128

    Article  Google Scholar 

  116. 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:e103592

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Schmuck R (2004) Effects of a chronic dietary exposure of the honeybee Apis mellifera (Hymenoptera: Apidae) to imidacloprid. Arch Environ Contam Toxicol 47:471–478

    Article  CAS  PubMed  Google Scholar 

  118. Schmuck R, Schöning R, Stork A, Schramel O (2001) Risk posed to honeybees (Apis mellifera L., Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 57:225–238

    Article  CAS  PubMed  Google Scholar 

  119. Schneider CW, Tautz J, Gruenewald B, Fuchs S (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS One 7:e30023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. 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 9:e91573

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  121. Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Cambridge

    Google Scholar 

  122. Smodis Skerl MI, Gregorc A (2010) Heat shock proteins and cell death in situ localisation in hypopharyngeal glands of honeybee (Apis mellifera carnica) workers after imidacloprid or coumaphos treatment. Apidologie 41:73–86

    Article  CAS  Google Scholar 

  123. Stanley DA, Raine NE (2016) Chronic exposure to a neonicotinoid pesticide alters the interactions between bumblebees and wild plants. Funct Ecol. doi:10.1111/1365-2435.12644

    PubMed  PubMed Central  Google Scholar 

  124. Stanley DA, Smith KE, Raine NE (2015) Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide. Sci Rep 5:16508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Stewart SD, Lorenz GM, Catchot AL, Gore J, Cook D, Skinner J, Mueller TC, Johnson DR, Zawislak J, Barber J (2014) Potential exposure of pollinators to neonicotinoid insecticides from the use of insecticide seed treatments in the mid-Southern United States. Environ Sci Technol 48:9762–9769

    Article  CAS  PubMed  Google Scholar 

  126. Stoner KA, Eitzer BD (2012) Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS One 7:e39114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Suchail S, Guez D, Belzunces LP (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem 20:2482–2486

    Article  CAS  PubMed  Google Scholar 

  128. Tan K, Chen W, Dong S, Liu X, Wang Y, Nieh JC (2015) A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Sci Rep 5:10989

    Article  PubMed  PubMed Central  Google Scholar 

  129. Tasei JN, Lerin J, Ripault G (2000) Sublethal effects of imidacloprid on bumblebees, Bombus terrestris (Hymenoptera: Apidae), during a laboratory feeding test. Pest Manag Sci 56:784–788

    Article  CAS  Google Scholar 

  130. Teeters BS, Johnson RM, Ellis MD, Siegfried BD (2012) Using video-tracking to assess sublethal effects of pesticides on honey bees (Apis mellifera L.). Environ Toxicol Chem 31:1349–1354

    Article  CAS  PubMed  Google Scholar 

  131. Thakur RK, Bienefeld K, Keller R (1997) Varroa defense behavior in A. mellifera carnica. Am Bee J 137:143–148

    Google Scholar 

  132. Thany SH, Gauthier M (2005) Nicotine injected into the antennal lobes induces a rapid modulation of sucrose threshold and improves short-term memory in the honeybee Apis mellifera. Brain Res 1039:216–219

    Article  CAS  PubMed  Google Scholar 

  133. Thompson HM, 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

    Article  CAS  Google Scholar 

  134. Thompson H, Coulson M, Ruddle N, Wilkins S, Harkin S (2016) Thiamethoxam: assessing flight activity of honeybees foraging on treated oilseed rape using radio frequency identification technology. Environ Toxicol Chem 35:385–393

    Article  CAS  PubMed  Google Scholar 

  135. Thompson HM, Wilkins S, Harkin S, Milner S, Walters KF (2015) Neonicotinoids and bumblebees (Bombus terrestris): effects on nectar consumption in individual workers. Pest Manag Sci 71:946–950

    Article  CAS  PubMed  Google Scholar 

  136. Tomé HVV, Martins GF, Lima MAP, Campos LAO, Guedes RNC (2012) Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS One 7:e38406

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  137. Van der Sluijs JP, Simon-Delso S, 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

    Article  Google Scholar 

  138. Van Dijk TC, Van Staalduinen MA, Van der Sluijs JP (2013) Macro-invertebrate decline in surface water polluted with imidacloprid. PLoS One 8:e62374

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  139. Vidau C, Diogon M, Aufauvre J, Fontbonne R, Vigues B, Brunet JL et al (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by nosema ceranae. PLoS One 6:e21550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336:351–352

    Article  CAS  PubMed  Google Scholar 

  141. Williamson SM, Baker DD, Wright GA (2013) Acute exposure to a sublethal dose of imidacloprid and coumaphos enhances olfactory learning and memory in the honeybee Apis mellifera. Invertebr Neurosci 13:63–70

    Article  CAS  Google Scholar 

  142. Williamson SM, Willis SJ, Wright GA (2014) Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology 23:1409–1418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Williamson SM, Wright GA (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 216:1799–1807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Wilson DE, Velarde RA, Fahrbach SE, Mommaerts V, Smagghe G (2013) Use of primary cultures of Kenyon cells from bumblebee brains to assess pesticide side effects. Arch Insect Biochem Physiol 84:43–56

    Article  CAS  PubMed  Google Scholar 

  145. Wu JY, Anelli CM, Sheppard WS (2011) Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS One 6:e14720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Xu T, Dyer DG, McConnell LL, Bondarenko S, Allen R, Heinemann O (2016) Clothianidin in agricultural soils and uptake into corn pollen and canola nectar after multi-year seed treatment applications. Environ Toxicol Chem 35:311–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Yang EC, Chang HC, Wu WY, Chen YW (2012) Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS One 7:e49472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the team of behavioral biology and biology education at the Ruhr-University for helpful discussions.

Author information

Authors and Affiliations

  1. Faculty of Biology and Biotechnology, Ruhr University Bochum, Universitätsstrasse 150, 44801, Bochum, Germany

    Abdulrahim T. Alkassab & Wolfgang H. Kirchner

Authors
  1. Abdulrahim T. Alkassab
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wolfgang H. Kirchner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdulrahim T. Alkassab.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alkassab, A.T., Kirchner, W.H. Sublethal exposure to neonicotinoids and related side effects on insect pollinators: honeybees, bumblebees, and solitary bees. J Plant Dis Prot 124, 1–30 (2017). https://doi.org/10.1007/s41348-016-0041-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41348-016-0041-0

Keywords

Search

Navigation