The synergy of xenobiotics in honey bee Apis mellifera: mechanisms and effects

Authors

  • Gordana Glavan
  • Janko Božič

DOI:

https://doi.org/10.14720/abs.56.1.15546

Keywords:

synergism, xenobiotic, Apis mellifera, mechanism, pesticide, P450

Abstract

During foraging activities honeybees are frequently exposed to different xenobiotics, most of them are agrochemical pesticides and beehive chemicals. Many pesticides are applied together and synergism is likely to occur in different organisms. The risk of synergisms is neglected and relatively few studies were performed concerning the effects and synergy mechanism of different xenobiotic combinations in honeybees. The understanding of synergy mechanisms between xenobiotics is very important for the control of defined mixtures use and also for the prediction of potential toxicity of newly developed substances in agriculture and apiculture. This review is focused on the effects, mechanisms and molecular targets of xenobiotics in honeybees and possible complex mechanisms of their synergisms. The main threat for honeybees are insecticides which primary molecular targets are few neuronal molecules therefore causing the impairment of neuronal system that have a profound effect on honeybee behavior, cognitive functions and physiology. However, the majority of synergistic effects observed in honeybees were ascribed to the inhibition of etoxifying midgut enzymes P450 involved in xenobiotic metabolism since most of studies were done with the mixtures xenobiotic/P450 inhibitor. The main inhibitors of P450 enzymes are specific compounds used to prolong the effects of pesticides as
well as some fungicides. Some insecticides can also interact with these enzymes and influence the xenobiotis. Although the primary mechanisms of action of individual xenobiotics especially insecticides are well known and there are possible interactions in honeybees at their primary target sites, this issue is underestimated and it warrants further investigation.

References

Barron, A.B., Maleszka, R., Vander Meer, R.K., Robinson, G.E., 2007. Octopamine modulates honey bee dance behavior. PNAS, 104 (5), 1703–1707. DOI: https://doi.org/10.1073/pnas.0610506104

Belzunces, L.P., Tchamitchian, S., Brunet, J.-L., 2012. Neural effects of insecticides in the honey bee. Apidologie, 43 (3), 348–370. DOI: https://doi.org/10.1007/s13592-012-0134-0

Bergougnoux, M., Treilho, U.M., Armengaud, C., 2013. Exposure to thymol decreased phototactic behavior in the honeybee (Apis mellifera) in laboratory conditions. Apidologie, 44(1), 88–89. DOI: https://doi.org/10.1007/s13592-012-0158-5

Bevk, D., Kralj, J., Čokl, A., 2012. Coumaphos affects food transfer between workers of honeybee Apis mellifera. Apidologie 43, 465–470. DOI: https://doi.org/10.1007/s13592-011-0113-x

Bicker, G., Schafer, S., Kingan, T.G., 1985. Mushroom body feedback interneurones in the honey bee show GABA-like immunoreactivity.Brain. Res., 360 (1-2), 394–397. DOI: https://doi.org/10.1016/0006-8993(85)91262-4

Blenau, W., Rademacher, E., Baumann, A., 2011. Plant essential oils and formamidines as insecticides/ acaricides: what are the molecular targets? Apidologie, 43 (3), 334–347. DOI: https://doi.org/10.1007/s13592-011-0108-7

Bloomquist, J.R., 2003. Chloride Channels as Tools for Developing Selective Insecticides. Archives of Insect Biochemistry and Physiology, 54 (4), 145–156. DOI: https://doi.org/10.1002/arch.10112

Boncristiani, H., Underwood, R., Schwarz, R., Evans, J.D., Pettis, J., vanEngelsdorp, D., 2012. Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. Journal of Insect Physiology, 58 (5), 613–620. DOI: https://doi.org/10.1016/j.jinsphys.2011.12.011

Burley, L., Fell, R., Saacke, R., 2008. Survival of honey bee (Hymenoptera: Apidae) spermatozoa incubated at room temperature from drones exposed to miticides. J. Econ. Entomol., 101 (4), 1081–1087. DOI: https://doi.org/10.1093/jee/101.4.1081

Cao, L.C., Honeyman, T.W., Cooney, R., Kennington, L., Scheid, C.R., Jonassen, J.A., 2004. Mitochondrial dysfunction is a primary event in renal cell oxalate toxicity. Kidney Int., 66 (5), 1890–1900. DOI: https://doi.org/10.1111/j.1523-1755.2004.00963.x

Casida, J.E., 2009. Pest toxicology: the primary mechanisms of pesticide action. Chem Res Toxicol., 22 (4), 609–619. DOI: https://doi.org/10.1021/tx8004949

Claudianos, C., Ranson, H., Johnson, R.M., Biswas, S., Schuler, M.A., Berenbaum, M.R., Feyereisen, R., and Oakeshott, J.G., 2006. A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol. Biol., 15 (5), 615–636. DOI: https://doi.org/10.1111/j.1365-2583.2006.00672.x

Cloyd, R.A., 2011. Pesticide Mixtures. In: Stoytcheva, M. (ed.): Pesticides-Formulations, Effects, Fate,InTech, pp. 69–80.

Coats, J.R., 1990. Mechanisms of toxic action and structure-activity relationships for organochlorine and synthetic pyrethroid insecticides. Environ. Health Perspect., 87, 255–262. DOI: https://doi.org/10.1289/ehp.9087255

Cole, L.M., Roush, R.T., Casida, J.E., 1993. Action of phenylpyrazole insecticides at the GABA-gated chloride channel. Pestic. Biochem. Physiol., 46 (1), 47–54. DOI: https://doi.org/10.1006/pest.1993.1035

Collins, A.M., Pettis, J.S., Wilbanks, R., Feldlaufer, M.F., 2004. Performance of honey bee (Apis mellifera) queens reared in beeswax cells impregnated with coumaphos. J. Apic. Res., 43 (3), 128–134. DOI: https://doi.org/10.1080/00218839.2004.11101123

Corbel, V., Stankiewicz, M., Bonnet, J., Grolleau, F., Hougard, J.M., Lapied, B., 2006. Synergism between insecticides permethrin and propoxur occurs through activation of presynaptic muscarinic negative feedback of acetylcholine release in the insect central nervous system. Neurotoxicology., 27 (4), 508–519. DOI: https://doi.org/10.1016/j.neuro.2006.01.011

Cully, D.F., Wilkinson, H., Vassilatis, D.K., Etter, A., Arena, J.P., 1996. Molecular biology and electrophysiology of glutamate-gated chloride channels of invertebrates. Parasitol., 113 (S1), S191–S200. DOI: https://doi.org/10.1017/S0031182000077970

Davies, T.G.E., Field, L.M., Usherwood, P.N.R., Williamson, M.S., 2007. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB-Life, 59 (3), 151–162. DOI: https://doi.org/10.1080/15216540701352042

Desneux, N., Decourtye, A., Delpuech, J.-M., 2007. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol., 52, 81–106. DOI: https://doi.org/10.1146/annurev.ento.52.110405.091440

Dudai, Y., Buxbaum, J., Corfas, G., Ofarim M., 1987. Formamidines interact with Drosophila octopamine receptors, alter the flies’ behaviour and reduce their learning ability. J. Comp. Physiol., 161 (5), 739–746. DOI: https://doi.org/10.1007/BF00605015

El Hassani, A.K., Dupuis, J.P., Gauthier, M., Armengaud, C., 2009. Glutamatergic and GABAergic effects of fipronil on olfactory learning and memory in the honeybee. Invertebrate Neuroscience, 9 (2), 91–100. DOI: https://doi.org/10.1007/s10158-009-0092-z

Ellis, M.D., Baxendale, F.P., 1997. Toxicity of seven monoterpenoids to tracheal mites(Acari: Tarsonemidae) and their honey bee (Hymenoptera: Apidae) hosts when applied as Fumigants. J. Econ. Entomol., 90 (5), 1087–1091. DOI: https://doi.org/10.1093/jee/90.5.1087

Elzen, P.J., Westervelt, D., 2002. Detection of coumaphos resistance in Varroa destructor in Florida. Am. Bee J., 142 (4), 291–292.

Enan, E., 2001. Insecticidal activity of essential oils: octopaminergic sites of action. Comparative Biochemistry and Physiology Part C, Toxicol. Pharmacol., 130 (3), 325–337. DOI: https://doi.org/10.1016/S1532-0456(01)00255-1

Enayati,A.A., Ranson, H., Hemingway, J., 2005. Insect glutathione transferases and insecticide resistance. Insect Molecular Biology, 14 (1), 3–8. DOI: https://doi.org/10.1111/j.1365-2583.2004.00529.x

Evans, P.D., Gee, J.D., 1980. Action of formamidine pesticides on octopamine receptors. Nature, 287 (5777), 60–62. DOI: https://doi.org/10.1038/287060a0

Floris, I., Satta, A., Cabras, P., Garau, V.L., Angioni, A., 2004. Comparison between two thymol formulations in the control of Varroa destructor: effectiveness, persistence, and residues. J. Econ. Entomol., 97 (2), 187–191. DOI: https://doi.org/10.1093/jee/97.2.187

Food and Agriculture Organization of the United Nations (FAO), 2009. FAOSTAT.http://faostat.fao.org

Fries, I., 1991. Treatment of sealed honey bee brood with formic acid for control of Varroa jacobsoni. Am. Bee J., 131 (5), 313–314.

Fukuto,T.R., 1990. Mechanism of action of organophosphorus and carbamate insecticides. Environ. Health Perspect., 87, 245–254. DOI: https://doi.org/10.1289/ehp.9087245

Georghiou, G.P., Atkins Jr. E.L., 1964. Temperature coefficients of toxicity of certain n-methyl carbamates against honeybees, and the effect of the synergist piperonyl butoxide. Journal of Apicultural Research, 3, 31–35. DOI: https://doi.org/10.1080/00218839.1964.11100079

Gregorc, A., Bowen, I., 2000. Histochemical characterization of cell death in honeybee larvae midgut after treatment with Paenibacillus larvae, amitraz and oxytetracycline. Cell. Biol. Int., 24 (5), 319–324. DOI: https://doi.org/10.1006/cbir.1999.0490

Gregorc, A., Smodisskerl, M.I., 2007. Toxicological and immunohistochemical testing of honeybees after oxalic acid and rotenone treatments.Apidologie, 38 (3), 296–305. DOI: https://doi.org/10.1051/apido:2007014

Gunasekara, A.S., Truong, T., Goh, K.S., Suprlock, F., Tjeerdema, R.S., 2007. Environmental fate and toxicology of fipronil. J. Pestic. Sci., 32 (3), 189–199. DOI: https://doi.org/10.1584/jpestics.R07-02

Haarmann, T., Spivak, M.,Weaver, D.,Weaver, B., Glenn, T., 2002. Effects of fluvalinate and coumaphos on queen honey bees (Hymenoptera: Apidae) in two commercial queen rearing operations. J. Econ. Entomol., 95 (1), 28–35. DOI: https://doi.org/10.1603/0022-0493-95.1.28

Hagler, J.R., Waller, G.D., Lewis, B.E., 1989. Mortality of honeybees Hymenoptera Apidae exposed to permethrin and combinations of permethrin with piperonyl butoxide. Journal of Apicultural Research, 28 (4), 208–211. DOI: https://doi.org/10.1080/00218839.1989.11101186

Hernández, A.F., Parrón, T., Tsatsakis, A.M., Requena, M., Alarcón, R., López-Guarnido, O., 2013. Toxic effects of pesticide mixtures at a molecular level: Their relevance to human health. Toxicology, 307, 136–145. DOI: https://doi.org/10.1016/j.tox.2012.06.009

Higes, M., Meana, A., Suarez, M., Llorente, J., 1999. Negative long-term effects on bee colonies treated with oxalic acid against Varroa jacobsoni Oud.. Apidologie, 30 (4), 289–292. DOI: https://doi.org/10.1051/apido:19990404

Homberg, U. 1994: Distribution of Neurotransmitters in the Insect Brain. Progress in Zoology, Vol. 40, Fischer, Stuttgart, 90 pp.

Iwasa, T., Motoyama, N., Ambrose, J.T., Roe, R.M., 2004. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection, 23 (5), 371–378. DOI: https://doi.org/10.1016/j.cropro.2003.08.018

Jeschke, P., Nauen,R., 2008. Neonicotinoids – from zero to hero in insecticide chemistry.Pest. Manag. Sci., 64 (11), 1084–1098. DOI: https://doi.org/10.1002/ps.1631

Johnson, R. M., Wen, Z., Schuler, M. A., Berenbaum,M. R., 2006. Mediation of Pyrethroid Insecticide Toxicity to Honey Bees (Hymenoptera: Apidae) by Cytochrome P450 Monooxygenases. Journal of Economic Entomology, 99(4), 1046–1050. DOI: https://doi.org/10.1093/jee/99.4.1046

Johnson, R.M., Pollock, H.S., Berenbaum, M.R., 2009. Synergistic interactions between in-hive miticides in Apis mellifera. J. Econ. Entomol., 102 (2), 474–479. DOI: https://doi.org/10.1603/029.102.0202

Johnson, R.M., Ellis, M.D., Mullin, C.A., Frazier, M., 2010. Pesticides and honey bee toxicity – USA. Apidologie, 41 (3), 312–331. DOI: https://doi.org/10.1051/apido/2010018

Johnson,R.M., Mao,W., Pollock,H.S., Niu,G., Schuler,M. A., Berenbaum,M. R., 2012. Ecologically Appropriate Xenobiotics Induce Cytochrome P450s in Apis mellifera. PLoS ONE, 7 (2), p. e31051. DOI: https://doi.org/10.1371/journal.pone.0031051

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: https://doi.org/10.1371/journal.pone.0054092

Jones, A.K., Sattelle,D.B., 2010. Diversity of Insect Nicotinic Acetylcholine Receptor Subunits: in Insect Nicotinic Acetylcholine Receptors. Advances in Experimental Medicine and Biology, 683, 25–43. DOI: https://doi.org/10.1007/978-1-4419-6445-8_3

Keyhani, J., Keyhani, E., 1980. EPR study of the effect of formate on cytochrome oxidase. Biochem. Biophys. Res. Comm., 92 (1), 327–333. DOI: https://doi.org/10.1016/0006-291X(80)91556-9

Kezic, N., Lucic, D., Sulimanovic, D., 1992. Induction of mixed function oxidase activity in honey bee as a bioassay for detection of environmental xenobiotics. Apidologie, 23 (3), 217–223. DOI: https://doi.org/10.1051/apido:19920304

Kral, K., 1980. Acetylcholinesterase in the ocellus of Apis mellifica. J. Insect Physiol. 26 (12), 807–809. DOI: https://doi.org/10.1016/0022-1910(80)90096-7

Kral, K., Schneider, L., 1981. Fine structural localization of acetylcholinesterase activity in the compound eye of the honeybee (Apis mellifica L.). Cell Tissue Res., 221 (2), 351–359. DOI: https://doi.org/10.1007/BF00216739

Kreissl, S., Bicker, G., 1989. Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J. Comp. Neurol., 286 (1), 71–84. DOI: https://doi.org/10.1002/cne.902860105

Kucharski, R., Ball, E.E., Hayward, D.C., Maleszka, R., 2000. Molecular cloning and expression analysis of a cDNA encoding a glutamate transporter in the honeybee brain. Gene, 244 (1–2), 399–405. DOI: https://doi.org/10.1016/S0378-1119(99)00503-X

Lienau , F.W., 1990. Effect of varroacide and pesticide treatment on honeybees. Apidologie, 21 (4), 375–377.

Liu, M.Y., Plapp, F.W. Jr, 1992. Mechanism of formamidine synergism of pyrethroids. Pestic. Biochem. Physiol., 43(2), 134–140. DOI: https://doi.org/10.1016/0048-3575(92)90027-W

Lodesani, M., Colombo, M., Spreafico, M., 1995. Ineffectiveness of Apistan® treatment against the mite Varroa jacobsoni Oud. in several districts of Lombardy (Italy). Apidologie, 26 (1), 67–72. DOI: https://doi.org/10.1051/apido:19950109

Locatelli, F., Bundrock, G., Müller, U., 2005. Focal and temporal release of glutamate in the mushroom bodies improves olfactory memory in Apis mellifera. Journal of Neuroscience, 25 (50), 11614–11618. DOI: https://doi.org/10.1523/JNEUROSCI.3180-05.2005

Maleszka, R., Helliwell, P., Kucharski, R., 2000. Pharmacological interference with glutamate re-uptake impairs long-term memory in the honeybee Apis mellifera. Behav. Brain. Res., 115 (1), 49–53. DOI: https://doi.org/10.1016/S0166-4328(00)00235-7

Mao, W., Rupasinghe, S.G., Johnson, R.M., Zangerl, A.R., Schuler, M.A., Berenbaum, M.R., 2009. Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comp. Biochem. Physiol. B Biochem. Mo.l Biol., 154 (4), 427–434. DOI: https://doi.org/10.1016/j.cbpb.2009.08.008

Mao, W., Schuler, M., Berenbaum, M., 2011. CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). PNAS, 108 (31), 12657–12662. DOI: https://doi.org/10.1073/pnas.1109535108

Mao,W., Schuler,M.A., Berenbaum,M.R., 2013. Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. PNAS, doi/10.1073/pnas.1303884110. DOI: https://doi.org/10.1073/pnas.1303884110

Marchetti, S., Barbattini, R., 1984. Comparative effectiveness of treatments used to control Varroa jacobsoni Oud.. Apidologie, 15 (4), 363–378. DOI: https://doi.org/10.1051/apido:19840401

Massoulie, L., Pezzementi, L., Bon, S., Krejci, E., Vallette, F.M.,1993. Molecular and cellular biology of cholinesterases. Prog. Neurobiol., 41 (1), 31–91. DOI: https://doi.org/10.1016/0301-0082(93)90040-Y

Meimaridou, E., Jacobson, J., Seddon, A.M., Noronha-Dutra, A.A., Robertson, W.G., Hothersal, J.S., 2005. Crystal and microparticle effects on MDCK cell superoxide production: oxalatespecific mitochondrial membrane potential changes. Free Radical Biology and Medicine, 38 DOI: https://doi.org/10.1016/j.freeradbiomed.2005.02.020

(12), 1553–1564.

Meled,M., Thrasyvoulou,A., Belzunces,L.P., 1998. Seasonal variations in susceptibility of Apis mellifera to the synergistic action of prochloraz and deltamethrin. Environmental Toxicology and Chemistry, 17 (12), 2517–2520. DOI: https://doi.org/10.1002/etc.5620171220

Meyer, E.P., Matute, C., Streit, P., Nässel, D.R., 1986. Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry, 84 (3), 207–216. DOI: https://doi.org/10.1007/BF00495784

Motoba, K., Suzuki, T., Uchida, M., 1992. Effect of a new acaricide, fenpyroximate, on energymetabolism and mitochondrial morphology in adult female Tetranychus urticae (two-spotted spider mite). Pestic. Biochem. Physiol, 43 (1), 37–44. DOI: https://doi.org/10.1016/0048-3575(92)90017-T

Narahashi, T., 1992. Nerve membrane Na+ channels as targets of insecticides. Trends. Pharmacol. Sci., 13 (6), 236–241. DOI: https://doi.org/10.1016/0165-6147(92)90075-H

Ortiz de Motellano, P.R., De Voss, J.J., 2005: Substrate oxidation by cytochrome P450 enzymes. In: Ortiz de Motellano, P.R. (ed.): Cytochrome P450, structure, mechanism, and biochemistry, Kluwer Academic/Plenum Publishers, New York. pp. 183–245. DOI: https://doi.org/10.1007/0-387-27447-2_6

Papaefthimiou, C., Theophilidis, G., 2001. The cardiotoxic action of the pyrethroid insecticide deltamethrin, the azole fungicide prochloraz and their synergy on the semi-isolated heart of the bee Apis mellifera macedonica. Pesticide Biochemistry and Physiology, 69 (2), 77–91. DOI: https://doi.org/10.1006/pest.2000.2519

Pettis, J.S., Collins, A.M.,Wilbanks, R., Feldlaufer, M.F., 2004. Effects of coumaphos on queen rearing in the honey bee, Apis mellifera. Apidologie, 35 (6), 605–610. DOI: https://doi.org/10.1051/apido:2004056

Pilling, E.D., 1992. Evidence for pesticide synergism is the honeybee (Apis mellifera). Aspects of Applied Biology, 31 (1), 43–47.

Priestley, C.M., Williamson, E.M., Wafford, K.A., Sattelle, D.B., 2003. Thymol, a constituent of thyme essential oil, is a positive allosteric modulator of human GABA(A) receptors and a homooligomeric GABA receptor from Drosophila melanogaster. British J. Pharmacol., 140 (8), 1363–1372. DOI: https://doi.org/10.1038/sj.bjp.0705542

Ray, D.E., Fry, J.R., 2006. A reassessment of the neurotoxicity of pyrethroid insecticides. Pharmacol. Ther., 111 (1), 174–93. DOI: https://doi.org/10.1016/j.pharmthera.2005.10.003

Raymond-Delpech, V., Matsuda, K., Sattelle, B.M., Rauh, J.J., Sattelle, D.B., 2005. Ion channels: molecular targets of neuroactive insecticides. Invertebr. Neurosci., 5 (3–4), 119–133. DOI: https://doi.org/10.1007/s10158-005-0004-9

Rinderer, T.E., De Guzman, L.I., Lancaster, V.A., Delatte, G.T., Stelzer, J.A., 1999. Varroa in the mating yard: I. The effects of Varroa jacobsoni and Apistan® on drone honey bees. Am. Bee J., 139 (3), 134–139.

Sattelle, D.B., 1980. Acetylcholine receptors of insects. Adv. Insect Physiol., 15, 215–315. DOI: https://doi.org/10.1016/S0065-2806(08)60142-3

Sattelle, D.B., Yamamoto, D., 1988. Molecular targets of pyrethroid insecticides. Adv. Insect Physiol., 20, 147–213. DOI: https://doi.org/10.1016/S0065-2806(08)60025-9

Schafer, S., Bicker, G., 1986. Distribution of GABA-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J. Comp. Neurol., 246 (3), 287–300. DOI: https://doi.org/10.1002/cne.902460302

Scheidler, A., Kaulen, P., Bruning, G.,Erber, J.,1990. Quantitative autoradiographic localization of [125I]alpha-bungarotoxin binding sites in the honeybee brain. Brain. Res., 534 (1–2), 332–335. DOI: https://doi.org/10.1016/0006-8993(90)90152-2

Schulz, D.J., Robinson, G.E., 2001. Octopamine influences division of labor in honey bee colonies. J. Compar. Physiol. A, 187 (1), 53–61. DOI: https://doi.org/10.1007/s003590000177

Scott, J.G., Wen Z.,2001. Cytochromes P450 of insects: the tip of the iceberg. Pest. Manag. Sci., 57 (10), 958–967. DOI: https://doi.org/10.1002/ps.354

Sherer, T.B., Richardson, J.R., Testa, C.M., Seo, B.B., Panov, A.V., Yagi, T., Matsuno-Magi, A., Miller, G.W., Greenamyre, J.T., 2007. Mechanism of toxicity of pesticides acting at complex I: relevance to environmental etiologies of Parkinson’s disease. J. Neurochem., 100 (6), 1469–1479.

Schmuck, R., Stadler, T., Schmidt, H.W., 2003. Field relevance of a synergistic effect observed in the laboratory between an EBI fungicide and a chloronicotinyl insecticide in the honeybee (Apis mellifera L, Hymenoptera). Pest Management Science, 59 (3), 279–286. DOI: https://doi.org/10.1002/ps.626

Sonnet, P.E., Lye, T.L., Sackett, R.R., 1978. Effects of selected herbicides on the toxicity of several insecticides to honey bees. Environ. Entomol., 7 (2), 254–256. DOI: https://doi.org/10.1093/ee/7.2.254

Song, C., Scharf, M.E., 2008. Formic acid: A neurologically active, hydrolyzed metabolite of insecticidal formate esters. Pestic. Biochem. Physiol., 92 (2), 77–82. DOI: https://doi.org/10.1016/j.pestbp.2008.06.005

Tasei, J.N., 2001. Effects of insect growth regulators on honey bees and non-apis bees. Apidologie, 32 (6), 527–545. DOI: https://doi.org/10.1051/apido:2001102

Tennekes, H.A., Sánchez-Bayo, F., 2013. The molecular basis of simple relationships between exposure concentration andtoxic effects with time. Toxicology, 309, 39–51. DOI: https://doi.org/10.1016/j.tox.2013.04.007

Thany, S.H., Tricoire-Leignel, H., Lapied, B., 2010. Identification of cholinergic synaptic transmission in the insect nervous system. Adv. Exp. Med. Biol., 683, 1–10. DOI: https://doi.org/10.1007/978-1-4419-6445-8_1

Thompson, H.M., 1996. Interactions between pesticides; a review of reported effects and their implications for wildlife risk assessment. Ecotoxicology, 5 (2), 59–81. DOI: https://doi.org/10.1007/BF00119047

Thompson, H.M., Wilkins, S., 2003. Assessment of the synergy and repellency of pyrethroid/fungicide mixtures. Bulletin of Insectology, 56 (1), 131–134.

Thompson, H.M., Wilkins, S., Battersby, A.H., Waite, R.J., Wilkinson, D., 2005. The effects of four insect growth regulating (IGR) insecticides on honeybee (Apis mellifera L.) colony development queen rearing and drone sperm production. Ecotoxicology, 14 (7), 757–769. DOI: https://doi.org/10.1007/s10646-005-0024-6

Thompson, H.M., 2012. Interaction between pesticides and other factors in effects on bees. http://www.efsa.europa.eu/en/supporting/doc/340e.pdf DOI: https://doi.org/10.2903/sp.efsa.2012.EN-340

Underwood, R., Currie, R., 2003. The effects of temperature and dose of formic acid on treatment efficacy against Varroa destructor (Acari: Varroidae), a parasite of Apis mellifera (Hymenoptera: Apidae). Exp. Appl. Acarol., 29 (3–4), 303–313.

Yu, S., Robinson, F., Nation, J., 1984. Detoxification capacity in the honey bee Apis mellifera L. Pestic Biochem Physiol, 22 (3), 360–368. DOI: https://doi.org/10.1016/0048-3575(84)90029-4

Vandame, R., Belzunces, L.P., 1998a. Erratum to “Joint actions of deltamethrin and azole fungicides on honey bee thermoregulation”.Neurosci Lett., 255 (1), 61. DOI: https://doi.org/10.1016/S0304-3940(98)00728-9

Vandame, R., Belzunces, L.P., 1998b. Joint actions of deltamethrin and azole fungicides on honey bee thermoregulation. Neurosci Lett., 251(1), 57–60. DOI: https://doi.org/10.1016/S0304-3940(98)00494-7

vanEngelsdorp, D., Meixner, M.D., 2010. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invertebr. Pathol., 103 (Suppl 1), S80–95. DOI: https://doi.org/10.1016/j.jip.2009.06.011

Weinberger, N.M., 2006. Food for Thought: Honeybee Foraging, Memory, and Acetylcholine. Sci. STKE, 336, p. pe23. DOI: https://doi.org/10.1126/stke.3362006pe23

Wheelock,C.E., Shan, G., Ottea, J., 2005. Overview of carboxylesterases and their role in the metabolism of insecticides. J. Pestic. Sci., 30 (2), 75–83. DOI: https://doi.org/10.1584/jpestics.30.75

Whittington, R., Winston, M.L., Melathopoulos, A.P., Higo, H.A., 2000. Evaluation of the botanical oils neem, thymol, and canola sprayed to control Varroa jacobsoni Oud. (Acari: Varroidae) and

Acarapsis woodi (Acari: Tarsonemidae) in colonies of honey bees (Apis mellifera L., Hymenoptera: Apidae). Am. Bee J., 140 (7), 565–572.

Wolstenholme, A.J., Rogers, A.T., 2005. Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology, 131 (Suppl S1), S85–S95. DOI: https://doi.org/10.1017/S0031182005008218

Zlotkin, E., 1999. The insect voltage-gated sodium channel as target of insecticides. Annu. Rev. Entomol., 44, 429–455. DOI: https://doi.org/10.1146/annurev.ento.44.1.429

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01.07.2013

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Original Research Paper

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Glavan, G., & Božič, J. (2013). The synergy of xenobiotics in honey bee Apis mellifera: mechanisms and effects. Acta Biologica Slovenica, 56(1), 11-25. https://doi.org/10.14720/abs.56.1.15546