The Effects of a systemic insecticide on stretching and production of wax in domestic bees Apis mellifera intermissa in Northen Africa (Algeria)

Authors

  • FATIMA TOUDERT-DJOUBER Department of Agronomic, Faculty of Biologic and Agronomic Sciences, University Mouloud Mammeri, Tizi-Ouzou, Algeria
  • V Plou Université de Toulouse, Institut National Universitaire Champollion, Place de Verdun, Albi, France
  • R Amrane Department of Agronomic, Faculty of Biologic and Agronomic Sciences, University Mouloud Mammeri, Tizi-Ouzou, Algeria
  • M Treilhou Université de Toulouse

DOI:

https://doi.org/10.17159/2254-8854/2022/a11116

Abstract

Imidacloprid is a well-known systemic insecticide which has a deleterious impact on honeybees. Beekeepers in the Tizi-Ouzou wilaya (Algeria) where the imidacloprid insecticide is used, report unusual losses and deaths of bee colonies. Even at sublethal doses, insecticid can impact the most crucial tasks of a bee colony such as comb building. This study was conducted in order to investigate the effect of an imidacloprid based insecticide (Confidor®Supra) on the production of wax by the honeybee Apis mellifera intermissa. After the imidacloprid LD50 was determined in controlled conditions, three sublethal doses were tested. The mortality, the syrup consumption and the weight of the wax generated were recorded.

The imidacloprid insecticide LD50 at 48 hours was evaluated at 3.5 ng.per bee on 4 days old spring worker bees. We found that the three sublethal doses (0.175 mg.L-1, 0.087 mg.L-1 and 0.035 mg.L-1) had an impact on the syrup consumption and the wax production by adult bees. Bees exposed to sublethal doses of insecticide consumed less syrup and produced less wax that the control bees. A dose response was observed regarding the production of wax.

The reduction of wax production by bees caused by an exposure to an imidacloprid based insecticide ads up to the many other effects of imidacloprid described in the literature.  This kind of impact could have harmful consequences for bee colonies as wax production is the basis of nest building. The physiological causes of the reduction of wax production remain to be investigated.

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References

Abbott WS. 1925. A method of computing the effectiveness of an insecticide. Journal of Economic Entomology. 18(2): 265–267. https://doi.org/10.1093/jee/18.2.265a.

ASSAF (Academy of Science of South Africa). 2021. Neonicotinoid insecticides: Use and effects in Africa Agriculture. A review and recommendations to policymakers. Proceedings report from a virtual event on Neonicotinoid Insecticides, held on 18 November 2020. Available at https://hdl.handle.net/20.500.11911/178.

Atkins EL, Kellum D. 1986. Comparative morphogenic and toxicity studies on the effect of pesticides on honeybee brood. Journal of Apicultural Research. 25(4): 242–255. https://doi.org/10.1080/00218839.1986.11100725.

Banerjee T, Banerjee D, Roy S, Banerjee H, Pal S. 2012. A comparative study on the persistence of imidacloprid and beta-cyfluthrin in vegetables. Bulletin of Environmental Contamination and Toxicology. 89(1): 193–196. https://doi.org/10.1007/s00128-012-0644-5.

Barker RJ, Lehner Y. 1974. Acceptance and sustenance value of naturally occurring sugars fed to newly emerged adult workers of honey bees (Apis mellifera L.). Journal of Experimental Zoology. 187(2): 277–285. https://doi.org/10.1002/jez.1401870211.

Barker RJ, Lehner Y. 1978. Laboratory comparison of high fructose cornsyrup, grape syrup, honey, and sucrose syrup as maintenance food for caged honey bees. Apidologie. 9(2): 111–116. https://doi.org/10.1051/apido:19780203.

Bendahou N, Fleche C, Bounias M. 1999. Biological and biochemical effects of chronic exposure to very low levels of dietary cypermethrin (Cymbush) on honeybee colonies (Hymenoptera : Apidae). Ecotoxicology and Environmental Safety. 44(2): 147–153. https://doi.org/10.1006/eesa.1999.1812.

Bonmatin JM, Moineau I, Charvet R, Fleche C, Colin ME, Bengsch ER. 2003. A LC/APCI-MS/MS method for analysis of imidacloprid in soils in plants, and in pollens. Analytical Chemistry. 75(9): 2027–2033. https://doi.org/10.1021/ac020600b.

Bonmatin JMB, Marchand PA, Charvet R, Moineau I, Bengsch ER, Colin ME. 2005. Quantification of imidacloprid uptake in maize crops. Journal of Agricultural and Food Chemistry. 53(13): 5336–5341. https://doi.org/10.1021/jf0479362.

Botias, C., David, A., Horwood, J., Abdul-Sada, A., Nicholls, E., Hill, E., & Goulson, D. 2015. Neonicotinoid residues in wildflowers, a potential route of chronic exposure for bees. Environmental Science &. Technology. 49, 21, 12731–12740. https://doi.org/10.1021/acs.est.5b03459.

CEBn°95,[Commission des Essais Biologiques] 1995. Méthode de laboratoire d’évaluation des effets de toxicité aigüe orale et de contact des préparations phytopharmaceutiques chez l’abeille domestique Apis melliferal L.

Chauvin R. 1976. Sur des substances qui provoquent l’étirage de la cire. Apidologie. 7(3): 237–242. https://doi.org/10.1051/apido:19760303.

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. Journal of Economic Entomology. 99(2): 253–262. https://doi.org/10.1093/jee/99.2.253.

Colin ME, Bonmatin JM, Moineau I, Gaimon C, Brun S, Vermandere JP. 2004. A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticides. Archives of Environmental Contamination and Toxicology. 47(3): 87–395. https://doi.org/10.1007/s00244-004-3052-y.

Darchen R. 1962. Observation directe du développement d’un rayon de cire. Le rôle des chaines d’abeilles. Insectes Sociaux. 9(2): 103–120. https://doi.org/10.1007/BF02224257.

Darchen R. 1980. La cire, son recyclage et son rôle probable à l’intérieur d’une colonie d’Apis mellifica. Apidologie. 11(3): 193–202. https://doi.org/10.1051/apido:19800301.

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 Management Science. 59(3): 269–278. https://doi.org/10.1002/ps.631.

Decourtye A, Le Metayer M, Pottiau H, Tisseur M, Odoux JF, Pham-Delegue MH. 2001. Impairment of olfactory learning performances in the honey bee after long term ingestion of imidaclopride (Avignon, France,1999). In: Belzunces LP, Pelissier C, Lewis GB, editors. Hazards of pesticides to bees. Paris: INRA (Les Colloques n°98). p. 113–118

Delabie J, Bos C, Fonta C, Masson C. 1985. Toxic and repellent effects of cypermethrin on the honeybee: Laboratory, glasshouse and field experiments. Pesticide Science. 16(4): 409–415. https://doi.org/10.1002/ps.2780160417.

DSA (Direction des Services Agricoles). 2016. Annuaire des statistiques agricoles de la wilaya de Tizi-Ouzou. Service des statistiques. Direction des Services Agricoles de la wilaya de Tizi-Ouzou.

DSA (Direction des Services Agricoles). 2018. Annuaire des statistiques agricoles de la wilaya de Tizi-Ouzou. Service des statistiques. Direction des Services Agricoles de la wilaya de Tizi-Ouzou.

Elbert A, Nauen R, Leicht W. 1998. Imidacloprid, a novel chloronicotinyl insecticide : biological activity and agricultural importance. In: Ishaaya I, Degheele D, editors. Insecticides with novel modes of action. Applied Agriculture. Berlin: Springer: p. 50–73. https://doi.org/10.1007/978-3-662-03565-8_4.

European and Mediterranean Plant Protection Organization (EPPO). 1992. Guideline on test methods for evaluating the side-effects of plant protection products on honeybees. EPPO Bulletin. 22: 203–215. https://doi.org/10.1111/j.1365-2338.1992.tb00483.x

Glinski Z, Kauko L. 2000. Immuno suppression et immuno toxicologie: aspects liés à la protection de l’abeille mellifère contre les agents microbiens et parasitaires. Apiacta. 35: 65–76.

Goulson D, Nicholls E, Botias C, Rotheray EL. 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. 347(6229): 1255957. https://doi.org/10.1126/science.255957.

Guez D. 2001. Sublethal effects of imidacloprid on honeybees behaviour (Apis mellifera). [Doctoral thesis]. Paris: Pierre et Marie Curie University.

Gupta PR, Chandel RS. Effects of diflubenzuron and penfluron on workers of Apis cerana indica F and Apis mellifera L. Apidologie (Celle). 1995;26(1):3–10. https://doi.org/10.1051/apido:19950101.

Halm MP, Rortais A, Arnold G, Tasei J, Rault S. New risk assessment approach for systemic insecticides : the case of Honey bees and imidacloprid (Gaucho). Environ Sci Technol. 2006;40(7):2448–2454. https://doi.org/10.1021/es051392i.

Hepburn HR, Hugo JJ, Mitchell D, Nijland MJM, Scrimgeour AG. 1984. On the energetic costs of wax production by the African honeybee, Apis mellifera adansonii. South African Journal of Science. 80(8): 363–368.

Hepburn HR, Muller WJ. 1988. Wax secretion in honeybees. Naturwissenschaften. 75(12): 628–629. https://doi.org/10.1007/BF00366481.

Hepburn HR, Bernard RTF, Davidson BC, Muller WJ, Lloyd P, Kurstjens SP, Vincent SL. 1991. Synthesis and secretion of beeswax in honeybees. Apidologie. 22(1): 21–36. https://doi.org/10.1051/apido:19910104.

Johansen CA, Mayer DF, Eves JD, Kious CW. 1983. Pesticides and bees. Environmental Entomology. 12(5): 1513–1518. https://doi.org/10.1093/ee/12.5.1513.

Kirchner WH. 1999. Mad-bee-disease? Sublethal effects of imidacloprid (Gaucho) on the behaviour of honeybees. Apidologie. 30(5): 421–422.

Lambin M, Armengaud C, Raymond S, Gauthier M. 2001. Imidacloprid induced facilitation of the proboscis extension reflex habituation in the honeybee. Archives of Insect Biochemistry and Physiology. 48(3): 129–134. https://doi.org/10.1002/arch.1065.

Ledoux MN, Winston ML, Higo H, Keeling CI, Slessor KN, LeConte Y. 2001. Queen and pheromonal factors influencing comb construction by simulated honey bee (Apis mellifera L.) swarms. Insectes Sociaux. 48(1): 14–20. https://doi.org/10.1007/PL00001738.

Nagata K, Ikeda T, Shono T. 1998. Modulation of the neuronal nicotinic acetylcholine receptor-channel by the nitromethylene heterocycle imidacloprid. Journal of Pharmacology and Experimental Therapeutics. 285(2): 731–738.

Nauen R, Hungenberg H, Tollo B, Tietjen K, Elbert A. 1998. Antifeedant effect, biological efficacy and high affinity binding of imidacloprid to acetylcholine receptors in Myzus persicae and Myzus nicotianae. Pest Management Science. 53(2): 133–140. https://doi.org/10.1002/(SICI)1096-9063(199806)53:23.0.CO;2-D.

Nauen R, Reckmann U, Armborst S, Stupp HP, Elbert A. 1999. Whitefly-active metabolites of imidacloprid: biological efficacy and translocation in cot- ton plants. Pest Management Science. 55(3): 265–271. https://doi.org/10.1002/(SICI)1096-9063(199903)55:33.0.CO;2-C.

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 Management Science. 57(7): 577–586. https://doi.org/10.1002/ps.331.

Pain J. 1966. Note technique nouveau modèle de cagettes expérimentales pour le maintien d’abeilles en captivité. Les Annales de l’Abeille. 9(1): 71–76.

Phytosanitary Inspection. 2016. Direction de la protection des végétaux et des contrôles techniques.

Pratt SC. 2004. Collective control of the timing and type of comb construction by honey bees (Apis mellifera) Stephen. Apidologie.; 35(2): 193–205. https://doi.org/10.1051/apido:2004005.

Püntener W. 1981. Manual for field trials in plant protection. 2nd ed. Basle: Ciba-Geigy Limited.

R Core Team. 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

Ramirez-Romero R, Chaufaux J, Pham-Delegue MH. 2005. 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(4): 601–611. https://doi.org/10.1051/apido:2005039.

Rortais A, Arnold G, Halm MP, Touffet-Briens 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. https://doi.org/10.1051/apido:2004071.

Sánchez-Bayo F, Tennekes HA. 2017. Assessment of ecological risks of agrochemicals requires a new framework. Environmental Risk Assessment and Remediation. 1(3): 1–9. https://doi.org/10.4066/2529-8046.100025.

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 Management Science. 57(3): 225–238. https://doi.org/10.1002/ps.270.

Scott-Durpee CD, Spivak MS. 2001. The impact of GAUCHO and TI-435 seed- treated canola on honeybees, Apis mellifera L. Bayer Corporation Report No. 110403, EPA MRID No. 45422435.

Suchail S, Guez D, Belzunces LP. 2000. Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environmental Toxicology and Chemistry. 19(7): 1901–1905. https://doi.org/10.1002/etc.5620190726.

Suchail S, Guez D, Belzunces LP. 2001. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera L. Environmental Toxicology and Chemistry. 20(11): 2482–2486. https://doi.org/10.1002/etc.5620201113

Suchail S, Debrauwer L, Belzunces LP. 2004. Metabolism of imidacloprid in Apis mellifera. Pest Management Science. 60(3): 291–296. https://doi.org/10.1002/ps.772.

Taranov GF. 1959. The production of wax in the honeybee colony. Bee World. 40(5): 113–121. https://doi.org/10.1080/0005772X.1959.11096711.

Vandame R, Meled M, Colin ME, Belzunces LP. 1995. Alteration of the homing-flight in the honey bee Apis mellifera L. exposed to sublethal dose of deltamethrin. Environmental Toxicology and Chemistry. 14(5): 855–860. https://doi.org/10.1002/etc.5620140517.

Whiffler LA, Hepburn HR. 1991. The queen in relation to wax secretion and comb building in honeybees. Journal of Comparative Physiology A. 169(2): 209–214. https://doi.org/10.1007/BF00215868.

Winston ML. 1991. The biology of the honey bee. Cambridge: Harvard University Press.

Wood TJ, Goulson D. 2017. The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environmental Science and Pollution Research. 24(21): 17285–17325. https://doi.org/10.1007/s11356-017-9240-x.

Zhu YC, Yao J, Adamczyk J, Luttrell R. 2017. Feeding toxicity and impact of imidacloprid formutation and mixtures with six representative pesticides at residue concentrations on hony bee physiology (Apis mellifera). PLoS One.;12(6):e0178421. https://doi.org/10.1371/journal.pone.0178421.

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Published

2022-10-27

How to Cite

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TOUDERT-DJOUBER F, Plou V, Amrane R, Treilhou M. The Effects of a systemic insecticide on stretching and production of wax in domestic bees Apis mellifera intermissa in Northen Africa (Algeria). Afr. Entomol. [Internet]. 2022 Oct. 27 [cited 2022 Nov. 29];30. Available from: https://www.africanentomology.com/article/view/11116

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