The risk exposure of bee colonies to the toxicity of systemic neonicotinoid insecticides was assessed. Various methods of chemical prevention of commercial winter and spring oilseed rape crops in field-realistic conditions were taken into account in the assessment. Pesticides were applied in accordance with the actual agricultural practice. Commercial crop protection products with thiamethoxam, clothianidin or imidacloprid were used as seed treatment. Formulations containing acetamiprid or thiacloprid were used for spraying. Fifteen healthy bee colonies were placed in close proximity to each of the oilseed rape fields throughout the blooming period. During florescence, the samples of nectar (directly from flowers and nectar flow from combs) and pollen loads were collected repeatedly. Samples of honey, bee bread and adult bees were taken one week after the end of plants flowering. To ensure high specificity and sensitivity of analysed pestcicides modified QuEChERS extraction method and liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS) was used. The five of neonicotinoid insecticides (imidacloprid, clothianidin, thiametoxam, acetamiprid and thiacloprid) were analyzed in multi-residue method with 0.1 - 10 ng/g limits of detection. Palynological analysis was done to determine the botanical origin of the nectar, honey and pollen. Development of bee colonies (brood area, worker biomass, colony health) was assessed every 3 weeks until the end of the beekeeping season. The amount of pollen collected by bees per hive, bee bread area and rape honey yield was also measured. The long-term effects of insecticides on bees were estimated using the same methods in April of the following year.
All the neonicotinoid insecticides applied to control oilseed rape pests were present in the samples of nectar and pollen. Their residue levels were lower than the acute oral and contact LD50 values. Among five examined neonicotinoids, the most frequently detected were: thiamethoxam, thiacloprid and acetamiprid. These substances were present in 65, 64, and 51% of the nectar samples and in 37, 62, and 45% of the pollen samples, respectively. The highest level of residues were noted after the thiamethoxam seed treatment; on average, 4.2 and 3.8 ng/g in the nectar and pollen samples. In the nectar and pollen samples from winter rape fields, lower levels of neonicotinoid residues were found in comparison to spring rape samples. The contaminations of neonicotinoids applied as seed dressing in nectar samples were significantly higher in comparison to the pollen samples. No negative effects of neonicotinoids on the bee mortality, brood development, strength, and honey yield of healthy bee colonies were found throughout the study period. However, the risk exposure of bee colonies on adverse impact of pesticide residues is high in areas of intensively cultivated oilseed rape.
If the inline PDF is not rendering correctly, you can download the PDF file here.
Alaux C. Brunet J. L. Dussaubat C. Mondet F. Tchamitchan S. Cousin M. Brillard J. Baldy A. Belzunces L. P. LeConte Y. (2010) - Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ.Microbiol. 12: 774-782.
Aliouane Y. Adessalam K. El Hassani A.K. Gary V. Armengaud C.Lambin M. Gauthier M. (2009) - Subchronic exposure of honeybees to sublethal doses of pesticides: effect on behavior. Environ. Toxicol. Chem. 28: 113-122.
Anastassiades M. Lehotay S. (2003) - Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “Dispersive Solid-Extraction” for the determination of pesticide residue in produce. J. AOAC Int. 86: 412-431.
Aufauvre J. Biron D. G. Vidau C. Fontbonne R. Roudel M. Diogon M. Vigues B. Belzunces L. P. Delbac F. Blot N. (2012) - Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honey bee. Sci. Rep. 2: 326.
Bailey J. Scott-Dupree C. Harris R. Tolman J. Harris B. (2005) - Contact and oral toxicity to honey bees (Apis mellifera) of agents registered for use for sweet corn insect control in Ontario Canada. Apidologie 36: 623-633.
Bernal J. Garrido-Bailon E. del Nozal M. J. Gonzalez-Porto A. V. Martin-Hernandez R. Diego J. C. Jimenez J. J. Bernal J. L. Higes M. (2010) - Overview of pesticide residues in stored pollen and their potential effect on bee colony (Apis mellifera) losses in Spain. J. Econ. Entomol. 103: 1964-1971.
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.
Chauzat M. P. Carpentier P. Martel A. C. Bougeard S. Cougoule N. Porta P. Lachaize J. Madec F. Aubert M. Faucon J. P. (2009) - Influence of pesticide residues on honey bee (Hymenoptera: Apidae) colony health in France. Environ. Entomol. 38: 514-523.
Chauzat M. P. Faucon J. P. Martel A. C. Lachaize J. Cougoule N. Aubert M. (2006) - A survey of pesticide residues in pollen loads collected by honey bees in France. J. Econ. Entomol. 99: 253-262.
Chauzat M. P. Martel A. C. Cougoule N. Porta P. Lachaize J. Zeggane S. Aubert M. Carpentier P. Faucon J. P. (2011) - An assessment of honeybee colony matrices Apis mellifera (Hymenoptera Apidae) to monitor pesticide presences in continental France. Environ.Toxicol. Chem. 30: 103-111.
Cutler G. C. Scott-Dupree C. D. (2007) - Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. J. Econ. Entomol. 100: 765-772.
Decourtye A. Armengaud C. Renou M. Devillers J. Cluzeau S.Gauthier M. Pham- Delègue M. H. (2004b) - Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pest. Biochem.Physiol. 78: 83-92.
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.
Decourtye A. Devillers J. Cluzeau S. Charreton M. Pham-Delègue M. H. (2004a) - Effects of imidacloprid and deltamethrin on associative learning in honeybees under semifield and laboratory conditions. Ecotoxicol.Environ. Saf. 57: 410-419.
Decourtye A. Devillers J. Genecque E. Le Menach K. Budzinski H. Cluzeau S. Pham Delègue M. H (2005) - Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch. Environ.Contam. Toxicol. 48: 242-250.
Decourtye A. Le Metayer M. Pottiau H. Tisseur M. Odoux J. F. Pham-Delègue M. H. (2001) - Impairment of olfactory learning performances in the honey bee after long term ingestion of imidacloprid. In Proceedings of the 7th International Symposium“Hazards of pesticides to bees”September7-9 1999 Avignon France. 98: 113-117.
Desneux N. Decourtye A. Delpuech J. M. (2007) - The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52: 81-106.
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 Journal 10(6): 2752.
Genersch E. von der Ohe W. Kaatz H. Schroeder A. Otten C. (2010) - The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41: 332-352.
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.
Henry M. Beguin M. Requier F. Rollin O. Odoux J. F. Aupinel P. Aptel J. Tchamitchian S. Decourtye A. (2012) - A common pesticide decreases for-aging success and survival in honey bees. Science 336(6079): 348-350. DOI: 10.1126/science.1215039.
Higes M. Martin-Hernandez R. Martinez-Salvador A. Garrido- Bailon E. Gonzalez-Porto A. V. Meana A. Bernal J. L. del Nozal M. J. Bernal J. (2010) - A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environ. Microbiol Rep. 2: 243-250.
Iwasa T. Motoyama N. Ambrose J. T. Roe M. R. (2004) - Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee Apis mellifera. Crop Prot. 23: 371-378.
Jabłoński B. (2002) - Notes on the method to investigate nectar secretion rate in flowers. J. Apic. Sci. 46(2): 117-125. Johnson R. M. Ellis M. D. Mullin C. A. Frazier M. (2010) - Pesticides and honey bee toxicity - U.S.A. Apidologie 41(3): 312-331.
Kołtowski Z. (2007) - Degree of utilization of potential sugar yield of a rapeseed plantation by insects inrespect of rapeseed honey yield in an apiary. J. Apic. Sci. 51(2): 67-79.
Krupke C. H. Hunt G. J. Eitzer B. D. Andino G. Given K. (2012) - Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7(1): e29268. DOI:10.1371/journal.pone.0029268.
Laurino D. Porporato M Patetta A. Manino A. (2011) - Toxicity of neonicotinoid insecticides to honey bees laboratory tests. Bull. Insectol. 64: 107-113.
Louveaux J. Maurizio A. Vorwohl G. (1978) - Methods of Melissopalynology. BeeWorld 59(4): 139-157.
Mullin C. A. Frazier M. Frazier J. L. Ashcraft S. Simonds R. (2010) - High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5(3): e9754. DOI: 10.1371 /journal.pone.0009754.
Nguyen B. K. Saegerman C. Pirard C. Mignon J. Widart J. Tuirionet B. Verheggen F. J. Berkvens D. De Pauw E. Haubruge E. (2009) - Does imidacloprid seed-treated maize have an impact on honey bee mortality? J. Econ.Entomol. 102: 616-623.
Pohorecka K. Bober A. Skubida M. Zdańska D. (2011) - Epizootic status of apiaries with massive losses of bee colonies (2008-2009). J. Apic. Sci. 55(1): 137-150.
Rortaisa A. Arnolda G. Halmb M. P. Touffet-Briensb F. (2005) - Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36(1): 71-83.
Schneider C. W. 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(1): e30023. DOI:10.1371/journal.pone.0030023.
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.
Tapparo A. Giorio C. Marzaro M. Marton D. Solda` L. Girolami V. (2011) - Rapid analysis of neonicotinoid insecticides in guttation drops of corn seedlings obtained from coated seeds. J. Environ. Monit. 13: 1564-1568.
Thompson H. M. Maus C. (2007) - The relevance of sublethal effects in honey bee testing for pesticide risk assessment. Pest.Manag. Sci. 63: 1058-1061.
Vidau C. Diogon M. Aufauvre J. Fontbonne R. Vigue`s B. Brunet J. L. Texier C. Biron D. G. Blot N. Alaoui H. E. Belzunces L. P. Delbac F. (2011) - Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosemaceranae. PLoS ONE 6: e21550.
Wallner K. Engl M. (2004) - Observations on bee colonies at rape seed fields seed dressed with different products. In Proceddings of Beesand Pesticides Symposium First EuropeanConference of Apidology Udine 19-23September 2004: 122-123.
Wiest L. Bulete A. Giroud B. Fratta C. Amic S. Lambert O. Poliquen H. Arnaudguilhem C. (2011) - Multi-residue analysis of 80 environmental contaminants in honeys honeybees and pollens by one extraction procedure followed by liquid and gas chromatography coupled with mass spectrometric detection. J. Chromatogr. A 1218: 5743-5756.
Yang E. C. Chuang Y. C. Chen Y. L. Chang L. H. (2008) - Abnormal foraging behaviour induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 101: 1743-1748.