The effects to honeybee colonies (Apis mellifera L.) during and after exposure to flowering maize (Zea mays L.), grown from seeds coated with clothianidin and imidacloprid was assessed in field-realistic conditions. The experimental maize crops were adjacent to the other flowering agriculture plants. Honey bee colonies were placed in three differently protected maize fields throughout the blooming period, and thereafter they were transferred to a stationary apiary. Samples of pollen loads, bee bread, and adult bees were collected and analyzed for neonicotinoid residues. To ensure high specificity and sensitivity of detection of the analyzed pesticides, a modified QuEChERS extraction method and liquid chromatography coupled with tandem mass spectrometry were used. Clothianidin was detected only in the samples of pollen loads. Their residue levels ranged from 10.0 to 41.0 ng/g (average 27.0 ng/g). Imidacloprid was found in no investigated sample. No negative effects of neonicotinoid seed-treated maize on the development and long-term survival of honey bee colonies were observed. The low proportion of Zea mays pollen in total bee-collected pollen during the maize flowering period was noted. The findings suggest that maize plants are less attractive forage for honey bees than phacelia (Phacelia tanacetifolia Benth.), buckwheat (Fagopyrum Mill.), white clover (Trifolium repens L.), goldenrod (Solidago L.), and vegetation from Brassicaceae family.
The results indicate a possibility of reducing the risk of bees being exposed to the toxic effect of insecticidal dusts dispersed during maize sowing by seeding, in the areas surrounding maize crops, plants that bloom later in the year.
If the inline PDF is not rendering correctly, you can download the PDF file here.
Aliouane Y., Adessalam K., El Hassani A. K., Gary V., Armengaud C., Lambin M., Gauthier M. (2009) Subchronic exposure of honey bees to sublethal doses of pesticides: effect on behavior. Environmental Toxicology and Chemistry 28:113-122.
Bortolotti L., Sabatini A. G., Mutinelli F., Astuti M., Lavazza A., Piro R., Tesoriero D., Medrzycki P., Sgolastra F., Porrini C. (2009) Spring honey bee losses in Italy. Julius Kühn Archiv 423: 148-151.
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 honey bee colony matrices, Apis mellifera (Hymenoptera Apidae) to monitor pesticide presences in continental France. Environmental Toxicology and Chemistry 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. Journal of Economic Entomology 100: 765-772.
Decourtye A., Devillers J. (2010) Ecotoxicity of neonicotinoid insecticides to bees. In: Thany S.H. (Ed.) Insect nicotinic acetylcholine receptors. Springer. New York. pp. 85-95.
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”. Avignon, France. 7-9 September 1999. 98: 113-117.
Decourtye A., Lacassie E., Pham-Delegue M. H. (2003) Learning performances of honey bees (Apis mellifera L.) are differentially affected by imidacloprid according to the season. Pest Management Science 59: 269-278.
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 honey bee Apis mellifera. Archives of Environmental Contamination and Toxicology 48: 242-250.
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 authorized in Europe. EFSA Journal 2012 10(6): 2752.
El Hassani A. K., Dacher M., Garry V., Lambin M., Gauthier M., Armengaud C. (2008) Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honey bee (Apis mellifera). Archives of Environmental Contamination and Toxicology 54: 653-661.
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.
Georgiadis P -Th., Pistorius J., Heimbach U., Stahler M., Schwabe K. (2012) Dust drift during sowing of maize - effects on honey bees. Julius Kühn Archiv 437: 134-139.
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. Journal of Economic Entomology 102: 1808-1815.
Greatti M., Barbattini R., Stravisi A., Sabatini A. G., Rossi S. (2006) Presence of the a.i. imidacloprid on vegetation near corn fields sown with Gaucho® dressed seeds. Bulletin of Insectology 59: 99-103.
Greatti M., Sabatini A. G., Barbattini R., Rossi S., Stravisi A. (2003) Risk of environmental contamination by the active ingredient imidacloprid used for corn seed dressing. Preliminary results. Bulletin of Insectology 56: 69-72.
Gregorc A., Ellis J. D. (2011) Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pest Biochemistry and Physiology 99: 200-207.
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 336(6079): 348-350. DOI: 10.1126/science.1215039
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 Protection 23: 371-378.
Johnson R. M., Dahlgren L., Siegfried B. D., Ellis M. D. (2013) Acaricide, Fungicide and Drug Interactions in Honey Bees (Apis mellifera). PLoS ONE 8(1): e54092. DOI:10.1371/journal.pone.0054092
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.
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. Bulletin of Insectology 64: 107-113.
Marzaro M., Vivan L., Targa A., Mazzon L., Mori N., Greatti M., Petrucco Toffolo E., di Bernardo A., Giorio C., Marton D.,Tapparo A., Girolami V. (2011) Lethal aerial powdering of honey bees with neonicotinoids from fragments of maize seed coat. Bulletin of Insectology 64(1): 119-126.
Mommaerts V., Reynders S., Boulet J., Besard L., Sterk G., Smagghe G., (2010) Risk assessment for sideeffects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19: 207-215.
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? Journal of Economic Entomology 102: 616-623.
Pistorius J., Bischoff G., Heimbach U., Stähler M. (2009) 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: 118-126.
Pohorecka K., Bober A., Skubida M., Zdańska D. (2011) Epizootic status of apiaries with massivelosses of bee colonies (2008-2009). Journal of Apicutural Science 55(1): 137-150.
Pohorecka K., Skubida P., Miszczak A., Semkiw P., Sikorski P., Zagibajło K., Teper D., Kołtowski Z., Skubida M., Zdańska D., Bober A. (2012) Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. Journal of Apicutural Science 56(2): 115-134. DOI: 10.2478/v10289-012-0029-3
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
Sgolastra F., Renzi T., Draghetti S., Scio C., Medrzycki P., Lodesani M, Maini S., Porrini C. (2012) Effects of neonicotinoid dust from maize seed-dressing on honeybees. Julius Kühn Archiv 437: 62.
Suchail S., Guez D., Belzunces L. P. (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environmental Toxicology and Chemistry 20: 2482-2486.