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Impacts of chronic sublethal exposure to clothianidin on winter honeybees

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Abstract

A wide application of systemic pesticides and detection of their residues in bee-collected pollen and nectar at sublethal concentrations led to the emergence of concerns about bees’ chronic exposure and possible sublethal effects on insect pollinators. Therefore, special attention was given to reducing unintentional intoxications under field conditions. The sensitivity of winter bees throughout their long lifespan to residual exposure of pesticides is not well known, since most previous studies only looked at the effects on summer bees. Here, we performed various laboratory bioassays to assess the effects of clothianidin on the survival and behavior of winter bees. Oral lethal and sublethal doses were administered throughout 12-day. The obtained LD50 values at 48, 72, 96 h and 10 days were 26.9, 18.0, 15.1 and 9.5 ng/bee, respectively. Concentrations <20 µg/kg were found to be sublethal. Oral exposure to sublethal doses was carried out for 12-day and, the behavioral functions were tested on the respective 13th day. Although slight reductions in the responses at the concentrations 10 and 15 µg/kg were observed, all tested sublethal concentrations had showed non-significant effects on the sucrose responsiveness, habitation of the proboscis extension reflex and olfactory learning performance. Nevertheless, chronic exposure to 15 µg/kg affected the specificity of the early long-term memory (24 h). Since the tested concentrations were in the range of field-relevant concentrations, our results strongly suggest that related-effects on winter and summer bees’ sensitivity should also be studied under realistic conditions.

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References

  • 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  Google Scholar 

  • Behrends A, Scheiner R (2010) Learning at old age: a study on winter bees. Front Behav Neurosci 4:15

    Google Scholar 

  • Blacquière T, Smagghe G, Gestel CAM, Mommaerts V (2012) Neonicotinoids in bees a review on concentrations side-effects and risk assessment. Ecotoxicology 21:973–992

    Article  Google Scholar 

  • 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  Google Scholar 

  • Cano Lozano V, Bonnard E, Gauthier M, Richard D (1996) Mecamylamine- induced impairment of acquisition and retrieval of olfactory conditioning in the honeybee. Behav Brain Res 81:215–222

    Article  Google Scholar 

  • Cano Lozano V, Armengaud C, Gauthier M (2001) Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. J Comp Physiol A 187:249–254

    Article  Google Scholar 

  • Ceuppens B, Eeraerts M, Vleugels T, Cnops G, Roldan-Ruiz I, Smagghe G (2015) Effects of dietary lambda-cyhalothrin exposure on bumblebee survival, reproduction, and foraging behavior in laboratory and greenhouse. J Pest Sci 88:777–783

    Article  Google Scholar 

  • Cox DR (1972) Regression models and life tables. Biometrics 38:67–77

    Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • Dacher M, Lagarrigue A, Gauthier M (2005) Antennal tactile learning in the honeybee: effect of nicotinic antagonists on memory dynamics. Neuroscience 130:37–50

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Decourtye A, Devillers J (2010) Ecotoxicity of neonicotinoid insecticides to bees. In: Thany SH (ed) Insect nicotinic acetylcholine receptors, 1st edn. Springer, New York, pp 85–95

    Chapter  Google Scholar 

  • 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(3):269–278

    Article  CAS  Google Scholar 

  • 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 

  • Decourtye A, Henry M, Desneux N (2013) Environment: overhaul pesticide testing on bees. Nature 497(7448):188

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • EFSA European Food Safety Authority (2013) Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin. EFSA J 11:3066

    Google Scholar 

  • 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  Google Scholar 

  • 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 

  • Gauthier M, Dacher M, Thany SH, Niggebrugge C, Deglise P, Kljucevic P, Armengaud C, Grünewald B (2006) Involvement of alpha-bungarotoxin- sensitive nicotinic receptors in long-term memory formation in the honeybee (Apis mellifera). Neurobiol Learn Mem 86:164–174

    Article  CAS  Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • Halm MP, Rortais A, Arnold G, Tasei JN, Rault S (2006) New risk assessment approach for systemic insecticides: the case of honey bees and imidacloprid (Gaucho). Environ Sci Technol 40:2448–2454

    Article  CAS  Google Scholar 

  • Hammer M, Menzel R (1995) Learning and memory in the honeybee. J Neurosci 15:1617–1630

    CAS  Google Scholar 

  • Han P, Niu CY, Lei CL, Cui JJ, Desneux N (2010a) 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  Google Scholar 

  • Han P, Niu CY, Lei CL, Cui JJ, Desneux N (2010b) Quantification of toxins in a Cry1Ac+ CpTI cotton cultivar and its potential effects on the honey bee Apis mellifera L. Ecotoxicology 19:1452–1459

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Joachimsmeier I, Pistorius J, Schenke D, Kirchner WH (2012) Guttation and risk for honey bee colonies (Apis mellifera L.): use of guttation drops by honey bees after migration of colonies—a field study. Julius-Kuhn-Archiv 437, 2012. In: 11th international symposium of the ICP-BR Bee Protection Group, Wageningen, 2–4 Nov 2011. doi: 10.5073/jka.2012.437.016

  • 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  Google Scholar 

  • 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  Google Scholar 

  • Laurino D, Manino A, Patetta A, Porporato M (2013) Toxicity of neonicotinoid insecticides on different honey bee genotypes. Bull Insectol 66:119–126

    Google Scholar 

  • Maus C, Curé G, Schmuck R (2003) Safety of imidacloprid seed dressings to honey bees: a comprehensive overview and compilation of the current state of knowledge. Bull Insectol 56:51–57

    Google Scholar 

  • McCabe SI, Hartfelder K, Santana WC, Farina WM (2007) Odor discrimination in classical conditioning of proboscis extension in two stingless bee species in comparison to Africanized honeybees. J Comp Physiol A 193:1089–1099

    Article  CAS  Google Scholar 

  • Ramirez-Romero R, Chaufaux J, Pham-delègue M (2005) Effects of Cry1Ab protoxin, deltametrhrin 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 

  • 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  Google Scholar 

  • Rundlöf M, Andersson GKS, Bommarco R, Fries I, Hederström V, Herbertsson L, Jonsson O, Klatt BK, Pedersen TR, Yourstone J et al (2015) Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521:77–80

    Article  Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • Schneider CW, Tautz J, Grünewald B, Fuchs S (2012) RFID Tracking of sub-lethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS One 7(1):e30023

    Article  CAS  Google Scholar 

  • Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV (2006) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc Natl Acad Sci USA 103:962–967

    Article  CAS  Google Scholar 

  • 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  Google Scholar 

  • Suchail S, Debrauwer L, Belzunces LP (2004) Metabolism of imidacloprid in Apis mellifera. Pest Manag Sci 60:291–296

    Article  CAS  Google Scholar 

  • Tennekes HA, Sánchez-Bayo F (2013) The molecular basis of simple relationships between exposure concentration and toxic effects with time. Toxicology 309:39–51

    Article  CAS  Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge

    Google Scholar 

  • Xu T, Dyer DG, McConnell LL, Bondarenko S, Allen R, Heinemann O (2015) Clothianidin in agricultural soils and uptake into corn pollen and canola nectar after multi-year seed treatment applications. Environ Toxicol Chem. Accepted doi:10.1002/etc.3281

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Acknowledgments

We thank the team of behavioral biology and biology education at the Ruhr-University for helpful discussions. We are also grateful to Dr. Pia Aumeier for her taking care of the study apiary. Suggestions and comments by anonymous reviewers and the editor to improve the manuscript are gratefully acknowledged.

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This study was not supported by any commercial company.

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

    Abdulrahim T. Alkassab & Wolfgang H. Kirchner

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  1. Abdulrahim T. Alkassab
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  2. Wolfgang H. Kirchner
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Correspondence to Abdulrahim T. Alkassab.

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Alkassab, A.T., Kirchner, W.H. Impacts of chronic sublethal exposure to clothianidin on winter honeybees. Ecotoxicology 25, 1000–1010 (2016). https://doi.org/10.1007/s10646-016-1657-3

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