Main Article Content
Honey bees are social insects produce honey and other hive products like propolis, royal jelly, bee venom and bee wax. Besides, their significance as the valued pollinators of many vegetable and horticultural crops they also play a crucial role in preservation of natural biodiversity. Many (diseases, parasites, insects) and environmental stress have an impact on the longevity and efficiency of honey bees. Gasses, heavy metals and air pollutants, in addition to inorganic compounds, have been linked to increased queen replacement and winter mortality in honey bees, as well as reduced brood survival and interference with cellular metabolism. Furthermore, natural poisons in food including toxic polysaccharides, phenolics, cyanogenic glycosides and alkaloids can impair colony performance, influence energy production via mitochondrial ATP synthase inhibition and result in acute mortality. In addition, adult bees ingesting acaricides such as formic acid and oxalic acid may die midgut cells, reducing bee activity, nursing behavior and longevity. Furthermore, biosphere pollution caused by irresponsible pesticide usage causing several issues to honey bee species, the most prominent of which is Apis mellifera L. Although no one chemical has been linked to colony collapse disorder, it is possible that it contributes to decreased honey bee health. Well understanding of pesticide mode of action in targeted pests and honey bees has resulted in a viable technique to prevent pesticide side effects on honey bees. As a result, the purpose of this review is to look into the toxicity of some pesticides used on crops, acaricides used in honey bee colonies and natural plant toxins. Understanding the role of these compounds and their side effects on honey bees is undoubtedly important in preventing colony collapse.
Alburaki M, Alburaki A. Morphometrical study on Syrian honey bees (Apis mellifera syriaca). Emirate Journal of Food and Agriculture. 2008;20(1):89-93.
Mishra RC. Honey bees and their management in India, publications and information division Indian council of agricultural research. Krishi Anusandhan Bhavan, Pusa, New Delhi. 1995;168.
Ibrahim MM, Chandel YS, Anil. Morphometrics of Apis mellifera after five decades of its introduction in North Western Himalayan region of India. Pakistan Journal of Zoology. 2017;49(4):1397-1403.
Harnaj V. Varroasis a honey bee diseases. Apimonodia Publications House. Bucharest. Romania.1977;91.
National Academy of Sciences. Status of pollinators in North America, National Academy Press. Washington DC; 2007.
Hardin MR, Benrey B, Coll M, Lamp WO, Roderick GK, Barbosa P. Arthropod pest resurgence: An overview of potential mechanisms. Crop Protection. 1995;14:3-18.
Ruberson JR, Nemoto H, Hirose Y. Pesticides and conservation of natural enemies in pest management. In: Barbosa P. (ed.) Conservation Biological Control. Academic Press, San Diego, CA. 1998;207-220.
Grosch DS. Reproductive performance of a braconid after heptachlor poisoning. Journal of Economic Entomology. 1970;63:1348-1349.
Rosenheim JA, Hoy MA. Sublethal effects of pesticides on the parasitoid aphytis melinus (Hymenoptera: Aphelinidae). Journal of Economic Entomology. 1988;81:476-483.
Rasuli F, Nazemi J, Sadeghi A. The acute oral toxicity of commonly used pesticides in Iran, to honey bees (Apis mellifera meda). Journal of Apiculture Sciences. 2014;59(1):17-26.
Akratanakul P. Pesticides and beekeeping. In Beekeeping in Asia. Rome: FAO Agricultural Ser¬vices Bulletin.1990;68-4.
Bortolotti L, Sabatini AG, Mutinelli F, Astuti M, Lavazza A, Piro R, Porrini C. Spring honey bee losses in Italy. Julius-Kühn Archiv. 2009;423:148-152.
European Food Safety Authority. Guidance on the risk assessment of plant protec¬tion products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA Journal. 2013;11(7):3295.
Pistorius J, Wehner A, Kriszan M, Bargen H, Knäbe S, Klein O, Frommberger M, Stähler M, Heimbach U. Application of predefined doses of neonicotinoid containing dusts in field trials and acute effects on honey bees. Bulletin of Insectology. 2015;68:161-172.
Quarles W. Pesticides and honey bee colony collapse disorder, IPM Practitioner. 2008;30:1-10.
Jeschke P, Nauen R. Neonicotinoids-from zero to hero in insecticide chemistry. Pest Management Science. 2008;64:1084-1098.
Cutler GC, Scott-Dupree CD, Drexler DM. Honey bees, neonicotinoids and bee incident reports: The Canadian situation. Pest Management Science. 2014;70(5):779-83.
Nguyen BK, Saegerman C. Pirard C, Mignon J, Widart J, Tuirionet B, Verheggen FJ, Berkvens D, De Pauw E, Haubruge E. Does imidacloprid seed-treated maize have an impact on honey bee mortality. Journal of Economic Entomology. 2009;102:616-623.
Suchail S, Guez D, Belzunces LP. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environmental Toxicological Chemistry. 2001;20:2482-2486.
Yang EC, Chuang YC, Chen YL, Chang, LH. Abnormal foraging behaviour induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology. 2008;101:1743-8.
Williamson SM, Willis SJ, Wright GA. Exposure to neonicotinoids influences the motor function of adult worker honey bees. Ecotoxicology. 2014;23(8):1409-18.
Tosi S, Burgio G, Nieh JC. A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Science Reports. 2017;7:1201.
Fischer J, Müller T, Spatz A-K, Greggers U, Grünewald B, Menzel R. Neonicotinoids Interfere with Specific Components of Navigation in Honeybees. PLoS ONE. 2014;9(3):e91364.
Tison L, Hahn ML, Holtz S, Rößner A, Greggers U, Bischoff G, Menzel R. Honey Bees’ behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field. Environmental Science and Technology. 2016;50(13):7218-7227.
Robinson WS, Nowogrodzki R, Morse RA. The value of honey bees as pollinators of US crops. II. American Bee Journal. 1989;129:477-487.
Wu MC, Chang YW, Lu KH, Yang EC. Gene expression changes in honey bees induced by sublethal imidacloprid exposure during the larval stage. Insect Biochemistry and Molecular Biology. 2017;88:12-20.
Bortolotti L, Montanari R, Marcelino J, Medrzycki P, Maini S, Porrini C. Effect of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bulletin of Insectology. 2003;56:63-67.
Ramirez-Romero R, Chaufaux J, Pham-Delegue M. Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honey bee Apis mellifera, a comparative approach. Apidologie. 2005;36(4):601-611.
Williamson SM, Wright GA. Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honey bees. Journal of Experimental Biology. 2013;216(10):1799-807.
Medrzycki P, Montanari R, Bortolotti L, Sabatini AG, Maini S, Porrini C. Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests. Bulletin of Insectology. 2003;56: 59-62.
Duan JJ, Marvier M, Huesing J, Dively G, Huang ZY. A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae), PLoSOne. 2008;3:e1415.
Malone LA, Burgess EP. Impact of genetically modified crops on pollinators. Environmental Impact of Genetically Modified Crops, ed. NFerry, AMR Gatehouse. 2009;199-224.
Soberon M, Gill S, Bravo A. Signaling versus punching hole: How do Bacillus thuringiensis toxins kill insect midgut cells. Cell Molecular Life Science. 2009;66: 1337-1349.
Bailey J, Scott Dupree C, Harris R, Tolman J, Harris B. Contact and oral toxicity to honey bees in Ontario, Canada, Apidologie. 2005;36:623-633.
Hardstone MC, Scott JG. Is Apis mellifera more sensitive to insecticides than other insects. Journal of Pest Management Science. 2010;66(11):1171-80.
Spurlock F, Lee M. Synthetic pyrethroid use patterns, properties, and environmental effects. In: Synthetic Pyrethroids: Occurrence and Behavior in Aquatic Environments (Gan J, Spurlock G, Hendley P, Weston D, Eds). ACS Symposium Series. 2008;3–25.
National Agricultural Statistics Service. Chemical use on fruit. United States Department of Agriculture, Sacramento. USA; 2012.
Ingram EM, Agustin J, Ellis MD, Siegfried BD. Evaluating sub-lethal effects of orchard-applied pyrethroids using video-tracking software to quantify honey bee behaviours. Chemosphere. 2015;135:272-277.
Oliver CJ, Softley S, Williamson SM, Stevenson PC, Wright GA. Pyrethroids and nectar toxins have subtle effects on the motor function, grooming and wing fanning behaviour of honey bees (Apis mellifera). PLoS ONE. 2015;10(8):1-12.
Decourtye A, Devillers J, Genecque E, Le Menach K, Budzinski H, Cluzeau S, et al. Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honey bee Apis mellifera. Archive of Environmental Contamination Toxicology. 2005;48(2):242–50.
Frost EH, Shutler D, Hillier NK. Effects of fluvalinate on honey bee learning, memory, responsiveness to sucrose, and survival. Journal Experimental Biology. 2013;216(15):2931-8.
Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R. High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One. 2010;5(3):e9754.
Pilon-Smits E. On the ecology of selenium accumulation in plants. Plants (Basel, Switzerland). 2019;8(7):197.
Johnson RM. Honey Bee Toxicology. Annual Review of Entomology. 2015;60:415-434.
Zhelyazkova I. Honey bees bioindicators for environmental quality, Bulgarian. Journal of Agricultural Science. 2010;18(3):435-442.
Ruschioni S, Paola R, Roxana L, Mariassunta S, Maddalena C, Claudio P, and Nunzio I. Biomonitoring with honey bees of heavy metals and pesticides in nature reserves of the marche region (Italy). Journal of Biological Trace Elements Research. 2010;1-8.
Al Naggar Y, Naiem EA, Seif AH, Mona MH. Honey bees and their products as a bio-indicator of environmental pollution with heavy metals, HARUM. 2013;13(26):10-20.
Thimmegowda GG, Brockmann A, Dhandapany PS, Olsson SB. Air pollution and health impacts on bees: Signs of causation. Proceedings of the National Academy of Sciences. 2020;17972.
Arpaia S, Imperatriz-Fonseca VL, Pires CSS, Silveira FS. Non-target and biodiversity impact on pollinators and flower visiting insects. In: Environmental risk assessment of genetically modified organisms: methodologies for assessing Bt cotton in Brazil. Ed. by Hilbeck A, Andow D, Fontes E, CABI Publishing, Cambridge. 2006;155–174.
Babendreier D, Romeis J, Bigler J, Fluri P. Neue erkenntnisse, zu möglichen auswirkungen von transgenem Bt-mais auf bienen, Forsch. Agroscope Liebefeld-Posieux ALP, Schweiz; 2006.
Pistorius J, Wehner A, Kriszan M, Bargen H, Knäbe S, Klein O, Heimbach U. Application of pre¬defined doses of neonicotinoid containing dusts in field trials and acute effects on honey bees. Bulletin of Insectology. 2015;68(2):161-172.
Harris J, Woodring J, John R. Effects of carbon dioxide on levels of biogentic amines in the brain of queenless worker and virgin queen honey bees (Apis mellifera). Journal of Apicultural Research. 1996;35(2): 69-78.
Porrini C, Ghini S, Girotti S, Sabatini A, Gattavecchia E, Medrxycki P, Grillenzoni F, Bortolotti L, Celli G. Honey bees and bee products as monitors of the environmental contamination. Apiacta. 2002;38:63-70.
Couvillon M, Ratnieks F. Environmental consultancy: Dancing bee bioindicators to evaluate landscape “health”, Frontiers in Ecology and Evolution. 2015;44(3):1-8.