Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris)

Pest Management Science

Volumn 70, Issue 2, 2014, Pages 332-337

  Cresswell, James E ^a,b   Robert, François Xavier L ^a   Florance, Hannah ^a   Smirnoff, Nicholas ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b UNIVERSITY OF CALCUTTA   (India)

Author keywords

Detoxification; Ecotoxicology; Insecticide; Oilseed rape; Pulse exposure; Recovery

Indexed keywords

BEE; BEHAVIORAL RESPONSE; CANOLA; CLEARANCE RATE; DETOXIFICATION; DOSE-RESPONSE RELATIONSHIP; ECOTOXICOLOGY; ENTOMOLOGY; IMIDACLOPRID; INGESTION RATE; LOCOMOTION; POLLUTION EXPOSURE;

APIS MELLIFERA; APOIDEA; BOMBUS TERRESTRIS; BRASSICA NAPUS;

IMIDACLOPRID; IMIDAZOLE DERIVATIVE; INSECTICIDE; NITRO DERIVATIVE; PESTICIDE RESIDUE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BEE; DETOXIFICATION; DRUG EFFECT; EATING; ECOTOXICOLOGY; METABOLISM; PULSE EXPOSURE; RAPESEED; RECOVERY; TIME;

DETOXIFICATION; ECOTOXICOLOGY; INSECTICIDE; OILSEED RAPE; PULSE EXPOSURE; RECOVERY;

ANIMALS; BEES; BEHAVIOR, ANIMAL; EATING; IMIDAZOLES; NITRO COMPOUNDS; PESTICIDE RESIDUES; TIME FACTORS;

EID: 84892482969     PISSN: 1526498X     EISSN: 15264998     Source Type: Journal    
DOI: 10.1002/ps.3569     Document Type: Article

References (45)

1. Elbert A, Haas M, Springer B, Thielert W and Nauen R, Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 64:1099-1105 (2008).
2. Nauen R and Jeschke P, Basic and applied aspects of neonicotinoid insecticides, in Green Trends in Insect Control, ed. by Lopez O and Fernandez-Bolanos JG. Royal Society of Chemistry, Cambridge, UK, pp. 132-162 (2011).
3. Rortais A, Arnold G, Halm MP and Touffet-Briens F, Modes of honeybee exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36:71-83 (2005).
4. Desneux N, Decourtye A and Delpuech JM, The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81-106 (2007).
5. Cresswell JE, A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:149-157 (2011).
6. Henry M, Beguin M, Requier F, Rollin O, Odoux J-F, Aupinel P et al., A common pesticide decreases foraging success and survival in honey bees. Science 336:348-350 (2012).
7. Laycock I, Lenthall KM, Barratt AT and Cresswell JE, Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21:1937-1945 (2012).
8. Whitehorn PR, O'Connor S, Wackers FL and Goulson D, Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336:351-352 (2012).
9. Existing Scientific Evidence of the Effects of Neonicotinoid Pesticides on Bees. [Online]. Environment Agency Austria. Available: http://www.europarl.europa.eu/committees/en/studiesdownload.html?file=79433&languageDocument=EN [11 March 2013].
10. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O and Kunin WE, Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345-353 (2010).
11. Blacquière T, Smagghe G, van Gestel CAM and Mommaerts V, Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973-992 (2012).
12. McCartney HA and Lacey ME, Wind dispersal of pollen from crops of oilseed rape (Brassica napus L.). J Aerosol Sci 22:467-477 (1991).
13. Brian A, Division of labour and foraging in Bombus agrorum Fabricius. J Anim Ecol 21:223-240 (1952).
14. Rodd FH, Plowright RC and Owen RE, Mortality rates of adult bumble bee workers (Hymenoptera: Apidae). Can J Zool Rev Can Zool 58:1718-1721 (1980).
15. Dukas R, Mortality rates of honey bees in the wild. Insectes Sociaux 55:252-255 (2008).
16. Rueppell O, Kaftanouglu O and Page R, Honey bee (Apis mellifera) workers live longer in small than in large colonies. Exp Gerontol 44:447-452 (2009).
17. Heinrich B, 'Majoring' and 'minoring' by foraging bumblebees, Bombus vagans: an experimental analysis. Ecology 60:245-255 (1979).
18. He YX, Zhao J, Zheng Y, Zhan Z, Desneux N and Wu KM, Lethal effect of imidacloprid on the coccinellid predator Serangium japonicum and sublethal effects on predator voracity and on functional response to the whitefly Bemisia tabaci. Ecotoxicology 21:1291-1300 (2012).
19. Nauen R, Behaviour modifying effects of low systemic concentrations of imidacloprid on Myzus persicae with special reference to an antifeeding response. Pestic Sci 44:145-153 (1995).
20. He Y, Zhao J, Wyckhuys K and Wu K, Sublethal effects of imidacloprid on Bemisia tabaci (Hemiptera: Aleyrodidae) under laboratory conditions. J Econ Entomol 104:833-838 (2011).
21. Azevedo-Pereira H, Lemos M and Soares A, Effects of imidacloprid exposure on Chironomus riparius Meigen larvae: linking acetylcholinesterase activity to behaviour. Ecotox Environ Safe 74:1210-1215 (2011).
22. Suchail S, De Sousa G, Rahmani R and Belzunces LP, In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L. Pest Manag Sci 60:1056-1062 (2004).
23. Suchail S, Debrauwer L and Belzunces LP, Metabolism of imidacloprid in Apis mellifera. Pest Manag Sci 60:291-296 (2004).
24. Wen ZM and Scott JG, Cross-resistance to imidacloprid in strains of German cockroach (Blattella germanica) and house fly (Musca domestica). Pestic Sci 49:367-371 (1997).
25. Ramirez-Romero R, Chaufaux J and Pham-Delegue MH, 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 (2005).
26. Tennekes H, The significance of the Druckrey-Küpfmüller equation for risk assessment-the toxicity of neonicotinoid insecticides to arthropods is reinforced by exposure time. Toxicology 276:1-4 (2010).
27. Maus C and Nauen R, Response to the publication: Tennekes, H.A. (2010): The significance of the Druckrey-Küpfmüller equation for risk assessment-the toxicity of neonicotinoid insecticides to arthropods is reinforced by exposure time. Toxicology 280:176-177 (2010).
28. Cresswell JE, Page C, Uygun M, Holmbergh M, Li Y, Wheeler J et al., Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology 115:365-371 (2012).
29. Armbruster DA, Tillman MD and Hubbs LM, Limit of detection (LQD)/limit of quantitation (LOQ): comparison of the empirical and the statistical methods exemplified with GC-MS assays of abused drugs. Clin Chem 40:1233-1238 (1994).
30. Liu ZW, Williamson MS, Lansdell SJ, Denholm I, Han ZJ and Millar NS, A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). P Natl Acad Sci USA 102:8420-8425 (2005).
31. Lind RJ, Clough MS, Reynolds SE and Earley FGP, [H-3]imidacloprid labels high- and low-affinity nicotinic acetylcholine receptor-like binding sites in the aphid Myzus persicae (Hemiptera: Aphididae). Pest Biochem Physiol 62:3-14 (1998).
32. Heinrich B, Thermoregulation in bumblebees. II. Energetics of warm-up and free flight. J Comp Physiol 96:155-166 (1975).
33. Tennekes H and Sanchez-Bayo F, Time-dependent toxicity of neonicotinoids and other toxicants: implications for a new approach to risk assessment. J Environ Anal Toxicol S4:001 (2011).
34. Deglise P, Grunewald B and Gauthier M, The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells. Neurosci Lett 321:13-16 (2002).
35. Ohno I, Tomizawaa M, Durkin KA, Casida JE and Kagabu S, Bis-neonicotinoid insecticides: observed and predicted binding interactions with the nicotinic receptor. Bioorg Med Chem Lett 19:3449-3452 (2009).
36. Shimomura M, Yokota M, Ihara M, Akamatsu M, Sattelle DB and Matsuda K, Role in the selectivity of neonicotinoids of insect-specific basic residues in loop D of the nicotinic acetylcholine receptor agonist binding site. Mol Pharmacol 70:1255-1263 (2006).
37. Bass C, Puinean AM, Andrews M, Cutler P, Daniels M, Elias J et al., Mutation of a nicotinic acetylcholine receptor beta subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neurosci 12:51.
38. Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M and Sattelle DB, Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573-580 (2001).
39. Matsuda K, Kanaoka S, Akamatsu M and Sattelle DB, Diverse actions and target-site selectivity of neonicotinoids: structural insights. Mol Pharmacol 76:1-10 (2009).
40. Buckingham SD, Lapied B, LeCorronc H, Grolleau F and Sattelle DB, Imidacloprid actions on insect neuronal acetylcholine receptors. J Exp Biol 200:2685-2692 (1997).
41. Rasmussen K and Czachura JF, Nicotine withdrawal leads to increased sensitivity of serotonergic neurons to the 5-HT1A agonist 8-OH-DPAT. Psychopharmacology 133:343-346 (1997).
42. Parker D, Serotonergic modulation of locust motor-neurons. J Neurophysiol 73:923-932 (1995).
43. Rueppell O, Hayworth MK and Ross NP, Altruistic self-removal of health-compromised honey bee workers from their hive. J Evol Biol 23:1538-1546.
44. Mommaerts V, Reynders S, Boulet J, Besard L, Sterk G and Smagghe G, Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19:207-215 (2010).
45. Stoughton SJ, Liber K, Culp J and Cessna A, Acute and chronic toxicity of imidacloprid to the aquatic invertebrates Chironomus tentans and Hyalella azteca under constant- and pulse-exposure conditions. Arch Environ Con Tox 54:662-673 (2008).