Neonicotinoid insecticides in pollen, honey and adult bees in colonies of the European honey bee (Apis mellifera L.) in Egypt
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Honeybee losses have been attributed to multiple stressors and factors including the neonicotinoid insecticides (NIs). Much of the study of hive contamination has been focused upon temperate regions such as Europe, Canada and the United States. This study looks for the first time at honey, pollen and bees collected from across the Nile Delta in Egypt in both the spring and summer planting season of 2013. There is limited information upon the frequency of use of NIs in Egypt but the ratio of positive identification and concentrations of NIs are comparable to other regions. Metabolites of NIs were also monitored but given the low detection frequency, no link between matrices was possible in the study. Using a simple hazard assessment based upon published LD50 values for individual neonicotinoids upon the foraging and brood workers it was found that there was a potential risk to brood workers if the lowest reported LD50 was compared to the sum of the maximum NI concentrations. For non-lethal exposure there was significant risk at the worst case to brood bees but actual exposure effects are dependant upon the genetics and conditions of the Egyptian honeybee subspecies that remain to be determined.
KeywordsHazard assessment Agriculture Honey bees Metabolites Imidacloprid LD50
The authors wish to acknowledge the support of grants Engineering Research Council of Canada (Project # 326415-07), Western Economic Diversification Canada (Project # 6578 and 6807), and an instrumentation grant from the Canada Foundation for Infrastructure and Meadow Ridge Enterprises LTD for providing apiaries and assistance with sampling and funding from the Saskatchewan Beekeepers Development Commission and Saskatchewan Agriculture through the Agriculture Development Commission to Dr. Albert Robertson.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no competing interests.
The bees used in this study were handled under the ethical guidelines of Tanta University Egypt, and all handling of hives was performed under the guidance and supervision of professional apiarists.
- Al Naggar YA, Naiem E-SA, Seif AI, Mona MH (2013) Honey bees and their products as a bio-in-dicator of environmental pollution with heavy metals Mellifera 13Google Scholar
- Al Naggar Y, Codling G, Giesy JP (2017) Human dietary intake and hazard characterization for residues of neonicotinoides and organophosphorus pesticides in Egyptian honey. Toxicol Environ Chem, 1–12. https://doi.org/10.1080/02772248.2017.1384828
- Chaplin-Kramer R et al. (2014) Global malnutrition overlaps with pollinator-dependent micronutrient production. In: Proc. R. Soc. B, 2014. The Royal Society, pp 1794–1799Google Scholar
- Cunningham S (2015) Honey bees in cotton a literature review of benefits to beekeepers and cotton growers. CSIRO Agricultural Productivity FlagshipGoogle Scholar
- DEFRA (2007) Assessment of the Risk Posed to Honeybees by Systemic Pesticides. Department for Environment, Food and Rural Affairs, London UKGoogle Scholar
- DEFRA (2009) Agriculture in the United Kingdom 2009. Department for Environment, Food and Rural Affairs, London UKGoogle Scholar
- Di Prisco G et al. (2013) Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc Natl Acad Sci 110:18466–18471. https://doi.org/10.1073/pnas.1314923110
- Engel MS (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis) J Hymenopt res 6:165–196Google Scholar
- EU Commission (2004) Review Report Acetamiprid. Health & Consumer Protection DirectorateGoogle Scholar
- Goulson D, Lye GC, DarvillB (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:1–542. https://doi.org/10.1146/annurev.ento.53.103106.093454 CrossRefGoogle Scholar
- Hassan AR (2009) Proceedings of the 4th COLOSS conference. Zagreb Croatia. doi:http://www.unep.org/dewa/Portals/67/pdf/Global_bee_colony_disorder _and_threats_insect_pollinators.pdfGoogle Scholar
- Kamel A (2010) Refined methodology for the determination of neonicotinoid pesticides and their metabolites in honey bees and bee products by liquid chromatography−tandem mass spectrometry (LC-MS/MS) J Agric Food Chem 58:5926–5931Google Scholar
- Kollmeyer WD, Flattum RF, Foster JP, Powell JE, Schroeder ME, Soloway SB (1999) Discovery of the nitromethylene heterocycle insecticides. In: Yamamoto I, JE C (eds) Nicotinoid insecticides and the nicotinic acetylcholine receptor. Springer, Tokyo, pp 71–89Google Scholar
- Laurino D, Manino A, Patetta A, Porporato M (2013) Toxicity of neonicotinoid insecticides on different honey bee genotypes. Bull Insect 66:119–126Google Scholar
- Lu C, Warchol KM, Callahan RA (2014) Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder. Bull Insect 67:125–130Google Scholar
- NASS NASS (2016) https://www.nass.usda.gov/index.php
- Nauen R, Ebbinghaus-Kintscher U, Schmuck R (2001) Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Manag Sci 57:577–586Google Scholar
- Pistorius J, Bischoff G, Heimbach U (2009) Bee poisoning by abrasion of active substances from seed treatment of maize during seeding in spring 2008. J Kult 61:9–14Google Scholar
- Sammataro D, Avitabile A (1998) The beekeeper’s handbook. Cornell University Press, Ithaca, USGoogle 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 57:225–238Google Scholar
- Shalaby SE, Abdou GY, Sallam AA (2012) Pesticide-residue relationship and its adverse effects on occupational workers in Dakahlyia, Egypt. Appl. Biol Res 14:24–32Google Scholar
- USEPA (2014) Guidance for assessing pesticide risks to bees. Washington, DCGoogle Scholar
- Yamada T, Yamada K, Wada N (2012) Influence of dinotefuran and clothianidin on a bee colony 臨床環境医学=. Jpn J Clin Ecol 21:10–23Google Scholar