Essential oils with the potential for varroa mite control (Varroa destructor): mechanisms of toxicity and negative impact on honey bee (Apis mellifera)
DOI:
https://doi.org/10.14720/abs.60.2.15682Keywords:
acaricides, essential oils, Apis mellifera, nervous system, immune system, varroa miteAbstract
The parasitic bee mite varroa (Varroa destructor) is among the most serious honey bee pests. Beekeepers utilize a wide range of different synthetic acaricides to keep mite populations under control. However, due to documented adverse impact of synthetic substances, the use of naturally derived acaricides, among these essential oils, is greatly being promoted. Thymol is already used in beekeeping. We present a review of the existing knowledge regarding the effects of essential oils on honey bees Apis mellifera. We focus only on those that have potential acaricide action. We discuss their mechanisms of toxic action on the immune and nervous systems. We conclude that due to their mechanisms of toxicity several essential oils could be used for varroa mite control, still very little data regarding the negative effects of essential oils on honey bees are known. In particular, knowing their interferences with the immune response is important to be able to predict the potential effect on the colony health. The majority of toxicity data currently exist for thymol and its commercial preparations under acute exposure (Apiguard®, Api Life VAR®), but the data for a
number of other potential acaricide-related essential oils are missing. We recognize the need for systematic screening of potential toxicity and sublethal effects of essential oils with acaricide action on honey bees. Standardised application of essential oils in
honey bee keeping remains a challenging task for the future.
References
Alayrangues, J., Hotier, L., Massou, I., Bertrand, Y., Armengaud, C., 2016. Prolonged effects of in-hive monoterpenoids on the honey bee Apis mellifera. Ecotoxicology, 25, 856-862. DOI: https://doi.org/10.1007/s10646-016-1642-x
Albo, G.N., Henning, C., Ringuelet, J., Reynaldi, F.J., De Giusti, M.R., Alippi, A.M., 2003. Evaluation of some essential oils for the control and prevention of American Foulbrood disease in honey bees. Apidologie, 34, 417-427. DOI: https://doi.org/10.1051/apido:2003040
Amdam, G.V., Simões, Z.L., Hagen, A., Norberg, K., Schrøder, K., Mikkelsen, Ø., Kirkwood, T.B., Omholt, S.W., 2004. Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Experimental Gerontology, 39(5), 767-773. DOI: https://doi.org/10.1016/j.exger.2004.02.010
Barbara, G.S., Zube, C., Rybak, J., Gauthier, M., Grünewald, B., 2005. Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural and Behavioral Physiology, 191, 823-836. DOI: https://doi.org/10.1007/s00359-005-0007-3
Bergougnoux, M., Treilhou, M., Armengaud, C., 2013. Exposure to thymol decreased phototactic behaviour in the honeybee (Apis mellifera) in laboratory conditions. Apidologie, 44, 82-89. DOI: https://doi.org/10.1007/s13592-012-0158-5
Barron, A.B., Maleszka, J., Vander Meer, R.K., Robinson, G.E., 2007. Octopamine modulates honey bee dance behavior. Proceedings of National Academy of Sciences USA, 104, 1703-1707. DOI: https://doi.org/10.1073/pnas.0610506104
Berry, J.A., Hood, W.M., Pietravalle, S., Delaplane, K.S., 2013. Field-level sublethal effects of approved bee hive chemicals on honey bees (Apis mellifera L). PLoS ONE, 8(10), e76536. DOI: https://doi.org/10.1371/journal.pone.0076536
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., 1999. Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microscopy Research and Techique, 45(3), 174-183. DOI: https://doi.org/10.1002/(SICI)1097-0029(19990501)45:3<174::AID-JEMT5>3.0.CO;2-U
Bicker, G., Schäfer, S., Kingan, T.G., 1985. Mushroom body feedback interneurons in the honey bee show GABA-like immunoreactivity. Brain Research, 360, 394-397. DOI: https://doi.org/10.1016/0006-8993(85)91262-4
Blenau, W., Rademacher, E., Baumann, A., 2012. Plant essential oils and formamidines as insecticides/ acaricides: what are the molecular targets? Apidologie, 43, 334-347. DOI: https://doi.org/10.1007/s13592-011-0108-7
Boncristiani, H., Underwood, R., Schwarz, R., Evans, J.D., Pettis, J., van Engelsdorp, D., 2012. Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. Journal of Insect Physiology, 58, 613-620. DOI: https://doi.org/10.1016/j.jinsphys.2011.12.011
Bonnafé, E., Alayrangues, J., Hotier, L., Massou, I., Renom, A., Souesme, G., Marty, P., Allaoua, M., Treilhou, M., Armengaud, C., 2017. Monoterpenoid-based preparations in beehives affect learning, memory, and gene expression in the bee brain. Environmental Toxicology and Chemistry, 36, 337-345. DOI: https://doi.org/10.1002/etc.3527
Burley, L.M., Fell, R.D., Saacke, R.G., 2008. Survival of honey bee (Hymenoptera: Apidae) spermatozoa incubated at room temperature from drones exposed to miticides. Journal of Economic Entomology, 101(4), 1081-1087. DOI: https://doi.org/10.1093/jee/101.4.1081
Burrell, B.D., Smith, B.H., 1995. Modulation of the honey bee (Apis mellifera) sting response by octopamine. Journal of Insect Physiology, 41, 671-680. DOI: https://doi.org/10.1016/0022-1910(95)00022-M
Cano Lozano, V., Bonnard, E., Gauthier, M., Richard, D., 1996. Mecamylamine-induced impairment of acquisition and retrieval of olfactory conditioning in the honeybee. Behavioural Brain Research, 81, 215-222. DOI: https://doi.org/10.1016/S0166-4328(96)89081-4
Cano Lozano, V., Bonnard, E., Gauthier, M., Richard, D., 2001. Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. Journal of Comparative Physiology. A, 187, 249-254. DOI: https://doi.org/10.1007/s003590100196
Carayon, J.L., Tene, N., Bonnafe, E., Alayrangues, J., Hotier, L., Armengaud, C., Treilhou, M., 2014. Thymol as an alternative to pesticides: Persistence and effects of Apilife Var on the phototactic behavior of the honeybee Apis mellifera. Environmental Science and Pollution Research, 21, 4934-4939. DOI: https://doi.org/10.1007/s11356-013-2143-6
Chaimanee, V., Evans, J.D., Chen, Y., Jackson, C., Pettis, J.S., 2016. Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos. Journal of Insect Physiology, 89, 1-8. DOI: https://doi.org/10.1016/j.jinsphys.2016.03.004
Chapman, R.F. 1998. Nervous system, The insects: structure and function, 5th ed. Cambridge University Press, Cambridge, 901 pp.
Cizelj, I., Glavan, G., Božič, J., Oven, I., Mrak, V., Narat, M., 2016. Prochloraz and coumaphos induce different gene expression patterns in three developmental stages of the Carniolan honey bee (Apis mellifera carnica Pollmann). Pesticide Biochemistry and Physiology, 128, 68-75. DOI: https://doi.org/10.1016/j.pestbp.2015.09.015
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. Journal of Apicultural Research, 43, 128-134. DOI: https://doi.org/10.1080/00218839.2004.11101123
Dai, P., Jack, C. J., Mortensen, A. N., Ellis, J. D., 2017. Acute toxicity of five pesticides to Apis mellifera larvae reared in vitro. Pest Management Science, doi:10.1002/ps.4608. DOI: https://doi.org/10.1002/ps.4608
Damiani, N., Gende, L.B., Bailac, P., Marcangeli, J.A., Eguaras, M.J., 2009. Acaricidal and insecticidal activity of essential oils on Varroa destructor (Acari: Varroidae) and Apis mellifera (Hymenoptera: Apidae). Parasitology Research, 106, 145-152. DOI: https://doi.org/10.1007/s00436-009-1639-y
Davies, T.G., Field, L.M., Usherwood, P.N., Williamson, M.S., 2007. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life, 59(3), 151-162. DOI: https://doi.org/10.1080/15216540701352042
Déglise, P., Grünewald, B., Gauthier, M., 2002. The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells. Neuroscience Letters, 321, 13-16. DOI: https://doi.org/10.1016/S0304-3940(01)02400-4
Desneux, N., Decourtye, A., Delpuech, J.M., 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52(1), 81-106. DOI: https://doi.org/10.1146/annurev.ento.52.110405.091440
Dietemann, V., Nazzi, F., Martin, S.J., Anderson, D.L., Locke, B., Delaplane, K.S., Wauquiez, Q., Tannahill, C., Frey, E., Ziegelmann, B., Rosenkranz, P., Ellis, J.D., 2013. Standard methods for varroa research, Journal of Apicultural Research, 52(1), 1-54. DOI: https://doi.org/10.3896/IBRA.1.52.1.09
Duay, P., de Jong, D., Engels, W., 2002. Decreased flight performance and sperm production in drones of the honey bee (Apis mellifera) slightly infested by Varroa destructor mites during pupal development. Genetics and Molecular Research, 1, 227-232.
Dudai, Y., Buxbaum, J., Corfas, G., Ofarim M., 1987. Formamidines interact with Drosophila octopamine receptors, alter the flies’ behaviour and reduce their learning ability. Journal of Comparative Physiology, 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. Journal of Economic Entomology, 90(5), 1087-1091. DOI: https://doi.org/10.1093/jee/90.5.1087
Enan, E., 2001. Insecticidal activity of essential oils: octopaminergic sites of action. Comparative Biochemitry and Physiology, C: Toxicology and. Pharmacology, 130, 325-337. DOI: https://doi.org/10.1016/S1532-0456(01)00255-1
Enan, E.E., 2005. Molecular response of Drosophila melanogaster tyramine receptor cascade to plant essential oils. Insect Biochemistry and Molecular Biology, 35, 309-321. DOI: https://doi.org/10.1016/j.ibmb.2004.12.007
Evans, J.D., Aronstein, K., Chen, Y.P., Hetru, C., Imler, J.L., Jiang, H., Hultmark D., 2006. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology, 15(5), 645-656. DOI: https://doi.org/10.1111/j.1365-2583.2006.00682.x
Evans, J.D. 2006. Beepath: An ordered quantitative-PCR array for exploring honey bee immunity and disease. Journal of Invertebrate Pathology, 93, 135-139. DOI: https://doi.org/10.1016/j.jip.2006.04.004
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
Farina, W.M., Wainselboim A.J., 2005. Trophallaxis within the dancing context: a behavioral and thermographic analysis in honeybees (Apis mellifera) Apidologie, 36, 43-47. DOI: https://doi.org/10.1051/apido:2004069
Farooqui, T. 2012. Review of octopamine in insect nervous systems. Open Access Insect Physiology, 4, 1-17. DOI: https://doi.org/10.2147/OAIP.S20911
Farooqui, T., Robinson, K., Vaessin, H., Smith, B.H. 2003. Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. Journal of Neuroscience, 23, 5370-5380. DOI: https://doi.org/10.1523/JNEUROSCI.23-12-05370.2003
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. Journal of Economic Entomology, 97(2), 187-191. DOI: https://doi.org/10.1093/jee/97.2.187
Fowler, M.A., Montell, C., 2013. Drosophila TRP channels and animal behavior. Life Sciences, 92(8-9), 394-403. DOI: https://doi.org/10.1016/j.lfs.2012.07.029
Fries, I., Hansen, H., Imdorf, A., Rosenkranz, P., 2003. Swarming in honey bees (Apis mellifera) and Varroa destructor population development in Sweden. Apidologie, 34, 389-398. DOI: https://doi.org/10.1051/apido:2003032
Fukuto, T.R, 1990. Mechanism of action of organophosphorus and carbamate insecticides. Environmental Health Perspectives, 87, 245-254. DOI: https://doi.org/10.1289/ehp.9087245
Garrido, P.M., Antúnez, K., Martín, M., Porrini, M.P., Zunino, P., Eguaras, M.J., 2013. Immune-related gene expression in nurse honey bees (Apis mellifera) exposed to synthetic acaricides. Journal of Insect Physiology, 59, 113-119. DOI: https://doi.org/10.1016/j.jinsphys.2012.10.019
Gashout, A.H., Guzmán-Novoa, E., 2009. Acute toxicity of essential oils and other natural compounds to the parasitic mite, Varroa destructor, and to larval and adult worker honey bees (Apis mellifera). Journal of Apicultural Research, 48, 263-269. DOI: https://doi.org/10.3896/IBRA.1.48.4.06
Ghasemi, V., Moharramipour, S., Tahmasbi, G., 2011. Biological activity of some plant essential oils against Varroa destructor (Acari: Varroidae), an ectoparasitic mite of Apis mellifera (Hymenoptera: Apidae). Experimental and Applied Acarology, 55, 147-154. DOI: https://doi.org/10.1007/s10493-011-9457-1
Gregorc, A., Bowen, I., 2000. Histochemical characterization of cell death in honeybee larvae midgut after treatment with Paenibacillus larvae, amitraz and oxytetracycline. Cell Biology International, 24, 319-324. DOI: https://doi.org/10.1006/cbir.1999.0490
Gregorc, A., Evans, J.D., Scharf, M., Ellis, J.D., 2012. Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor). Journal of Insect Physiology, 58(8), 1042-1049. DOI: https://doi.org/10.1016/j.jinsphys.2012.03.015
Grohmann, L., Blenau, W., Erber, J., Ebert, P.R., Strünker, T., Baumann, A., 2003. Molecular and functional characterization of an octopamine receptor from honeybee (Apis mellifera) brain. Journal of Neurochemistry, 86, 725-735. DOI: https://doi.org/10.1046/j.1471-4159.2003.01876.x
Grünewald, B., 1999. Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera. Journal of Comparative Neurology, 404(1), 114-126. DOI: https://doi.org/10.1002/(SICI)1096-9861(19990201)404:1<114::AID-CNE9>3.0.CO;2-#
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. Journal of Economic Entomology, 95, 28-35. DOI: https://doi.org/10.1603/0022-0493-95.1.28
Hammer, M., Menzel, R., 1998. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learning and Memory, 5, 146-156. DOI: https://doi.org/10.1101/lm.5.1.146
Heisenberg, M., 1998. What do the mushroom bodies do for the insect brain? An introduction. Learning and Memory, 5 (1-2), 1-10. DOI: https://doi.org/10.1101/lm.5.1.1
Hildebrand, J.G., ,Shepherd, G.M., 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annual Review of Neuroscience, 20, 595-631. DOI: https://doi.org/10.1146/annurev.neuro.20.1.595
Hillyer, J.F., 2016. Insect immunology and hematopoiesis. Developmental and Comparative Immunology, 58, 102-118. DOI: https://doi.org/10.1016/j.dci.2015.12.006
HMA, Heads of Medicines Agencies, 2015. http://www.hma.eu/uploads/media/Questionnaire_-_Bee_products_in_EU_EE_update_06.03.15.pdf
Imdorf, A., Bogdanov, S., Ibáñez Ochoa, R., Calderone, N.W., 1999. Use of essential oils for the control of Varroa jacobsoni Oud. in honey bee colonies. Apidologie, 30, 209-228. DOI: https://doi.org/10.1051/apido:19990210
Imdorf, A., Kilchenmann, V., Bogdanov, S., Bachofen, B., Beretta, C., 1995. Toxic effects of thymol, camphor, menthol and eucalyptol on Varroa jacobsoni Oud and Apis mellifera L in a laboratory test. Apidologie, 26, 27-31. DOI: https://doi.org/10.1051/apido:19950104
James, R.R., Xu, J., 2012. Mechanisms by which pesticides affect insect immunity. Journal of Invertebrate Pathology, 109, 175-182. DOI: https://doi.org/10.1016/j.jip.2011.12.005
Johnson, R.M., Ellis, M.D., Mullin, C.A., Frazier, M., 2010. Pesticides and honey bee toxicity - USA. Apidologie, 41, 312-331. DOI: https://doi.org/10.1051/apido/2010018
Kakumanu, M.L., Reeves, A.M., Anderson, T.D., Rodrigues, R.R., Williams, M.A., 2016. Honey bee gut microbiome is altered by in-hive pesticide exposures. Frontiers in Microbiology, 7, 1255. DOI: https://doi.org/10.3389/fmicb.2016.01255
Kenyon, F.C., 1896. The meaning and structure of the so-called „mushroom bodies“ of the hexapod brain. American Naturalist, 356 (30), 643-650. DOI: https://doi.org/10.1086/276450
Koul, O., Walia, S., Dhaliwal, G. S., 2008. Essential oils as green pesticides: potential and constraints. Biopesticides International, 4(1), 63-84.
Kral, K., 1980. Acetylcholinesterase in the ocellus of Apis mellifica. Journal of Insect Physiology, 26, 807-809. DOI: https://doi.org/10.1016/0022-1910(80)90096-7
Kral, K., Schneider, L., 1981. Fine structural localisation of acetylcholinesterase activity in the compound eye of the honeybee (Apis mellifica L.). Cell and Tissue Research, 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. Journal of Comparative Neurology, 286 (1), 71-84. DOI: https://doi.org/10.1002/cne.902860105
Kreissl, S., Eichmüller, S., Bicker, G., Rapus, J., Eckert, M., 1994. Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. Journal of Comparative Neurology, 348(4), 583-595. DOI: https://doi.org/10.1002/cne.903480408
Lindberg, C.M., Melathopoulos, A.P., Winston, M.L., 2000. Laboratory evaluation of miticides to control Varroa jacobsoni (Acari: Varroidae), a honey bee (Hymenoptera: Apidae) parasite. Journal DOI: https://doi.org/10.1603/0022-0493-93.2.189
of Economic Entomology, 93, 189-198.
Menzel, R., 2001. Searching for the memory trace in a mini-brain, the honeybee. Learning and Memory, 8 (2), 53-62. DOI: https://doi.org/10.1101/lm.38801
Mercer, A.R., Mobbs, P.G., Davenport, A.P., Evans, P.D., 1983. Biogenic amines in the brain of the honeybee, Apis mellifera. Cell and Tissue Research, 234, 655-677. DOI: https://doi.org/10.1007/BF00218658
Marchetti, S., Barbattini, R., D’Agaru, M., 1984. Comparative effectiveness of treatments used to control Varroa jacobsoni Oud. Apidologie, 15 (4), 363-378. DOI: https://doi.org/10.1051/apido:19840401
Meyer, E.P., Matute, C., Streit, P., Nässel, D.R., 1986. Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry, 84, 207-216. DOI: https://doi.org/10.1007/BF00495784
Mobbs. P.G., 1982. The Brain of the Honeybee Apis Mellifera. I. The Connections and Spatial Organization of the Mushroom Bodies. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 298 (1091), 309-354. DOI: https://doi.org/10.1098/rstb.1982.0086
Mobbs, P.G., 1985. Brain structure. In: Kerkut, G., Gilbert, L.I. (eds.): Comprehensive insect physiology pharmacology and biochemistry, 1st ed. Pergamon Press, Oxford, pp 299-370.
Mondet, F., Goodwin, M., Mercer, A., 2011. Age-related changes in the behavioural response of honeybees to Apiguard®, a thymol-based treatment used to control the mite Varroa destructor. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural and Behavioral Physiology, 197, 1055-1062. DOI: https://doi.org/10.1007/s00359-011-0666-1
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, 577-586. DOI: https://doi.org/10.1002/ps.331
OECD, Test No. 245: Honey Bee (Apis Mellifera L.), Chronic Oral Toxicity Test (10-Day Feeding).
http://www.oecd.org/env/ehs/testing/test-no-245-honey-bee-apis-mellifera-l-chronic-oral-toxicity-test-10-day-feeding-9789264284081-en.htm (dostop 23.11.2017)
Oruc, H.H., Hranitz, J. M., Sorucu, A., Duell, M., Cakmak, I., Aydin, L., Orman, A., 2012. Determination of acute oral toxicity of flumethrin in honey bees. Journal of Economic Entomology, 105 (6), 1890-1894. DOI: https://doi.org/10.1603/EC12055
Pettis, J.S., Collins, A., Wilbanks ,R., 2004. Effects of coumaphos on queen rearing in the honey bee, Apis mellifera. Apidologie, 35, 605-610. DOI: https://doi.org/10.1051/apido:2004056
Rejski program za kranjsko čebelo (2011-2015), 2010. http://www.czs.si/.HMA, 2015. http://www.hma.eu/uploads/media/Questionnaire_-_Bee_products_in_EU_EE_update_06.03.15.pdf;
Roma, G. C., Bueno, O. C., Camargo-Mathias, M. I., 2010. Morpho-physiological analysis of the insect fat body: a review. Micron, 41, 395-401. DOI: https://doi.org/10.1016/j.micron.2009.12.007
Rosenkranz, P., Aumeier, P., Ziegelmann, B., 2010. Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, Suppl 1, S96-119. DOI: https://doi.org/10.1016/j.jip.2009.07.016
Rybak, J., Menzel, R., 1993. Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. Journal of Comparative Neurology, 334(3), 444-465. DOI: https://doi.org/10.1002/cne.903340309
Rybak, J., Menzel, R., 1998. Integrative properties of the Pe1 neuron, a unique mushroom body output neuron. Learning and Memory, 5(1-2), 133-145. DOI: https://doi.org/10.1101/lm.5.1.133
Sachse, S., Galizia, C.G., 2002. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. Journal of Neurophysiology, 87(2), 1106-1117. DOI: https://doi.org/10.1152/jn.00325.2001
Sammataro, D., Finley, J., LeBlanc, B., Wardell, G., Ahumada-Segura, F., Carroll, M.J., 2009. Feeding essential oils and 2-heptanone in sugar syrup and liquid protein diets to honey bees (Apis mellifera L.) as potential Varroa mite (Varroa destructor) controls. Journal of Apiculture Research, 48, 256-262. DOI: https://doi.org/10.3896/IBRA.1.48.4.05
Sánchez-Bayo, F., Goulson, D., Pennacchio, F., Nazzi, F., Goka, K., Desneux, N., 2016. Are bee diseases linked to pesticides? - A brief review. Environmental International, 89-90, 7-11. DOI: https://doi.org/10.1016/j.envint.2016.01.009
Schafer, S., Bicker, G., 1986. Distribution of GABA-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. Journal of Comparative Neurology, 246, 287-300. DOI: https://doi.org/10.1002/cne.902460302
Schäfer, S., Bicker, G., 1986. Common projection areas of 5-HT- and GABA-like immunoreactive fibers in the visual system of the honeybee. Brain Research, 380(2), 368-370. DOI: https://doi.org/10.1016/0006-8993(86)90237-4
Scheidler, A., Kaulen, P., Brüning, G., Erber J., 1990. Quantitative autoradiographic localization of [125I]alpha-bungarotoxin binding sites in the honeybee brain. Brain Research, 534 (1-2), 332-335. DOI: https://doi.org/10.1016/0006-8993(90)90152-2
Schmehl, D.R., Teal, P.E., Frazier, J.L., Grozinger, C.M., 2014. Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera). Journal of Insect Physiology, 71, 177-190. DOI: https://doi.org/10.1016/j.jinsphys.2014.10.002
Schneider, C., Bevk, D., Grünewald, B., Tautz, J., Fuchs, S., 2009. Radiofrequency identification. Apidologie, 40, 659-660.
Schürmann, F.W., 1970. Structure of the mushroom bodies of the insect brain. I. Synapses in the peduncle. Zeitschritt fur Zellforschung and Mikroskopische Anatomie, 103(3), 365-381. DOI: https://doi.org/10.1007/BF00335280
Schwaerzel, M., Monastirioti, M., Scholz, H., Friggi-Grelin, F., Birman, S., Heisenberg, M., 2003. Dopamine and octopaminergic differentiate between aversive and appetitive olfactory memories in Drosophila. Journal of Neuroscience, 23, 10495-10502. DOI: https://doi.org/10.1523/JNEUROSCI.23-33-10495.2003
Smodis Skerl, M.I.S., Gregorc, A., 2010. Heat shock proteins and cell death in situ localisation in hypopharyngeal glands of honeybee (Apis mellifera carnica) workers after imidacloprid or coumaphos treatment. Apidologie, 41, 73-86. DOI: https://doi.org/10.1051/apido/2009051
Thany, S.H., Tricoire-Leignel, H., Lapied, B., 2010. Identification of cholinergic synaptic transmission in the insect nervous system. Advances in Experimental Medicine and Biology, 683, 1-10. DOI: https://doi.org/10.1007/978-1-4419-6445-8_1
Van Buren, N.W.M., Mariën, A.GH., Oudejans, R.C.H.M., Velthuis., H.H.W., 1992. Perizin, an acaricide to combat the mite Varroa jacobsoni its distribution in and influence on the honeybee Apis mellifera. Physiological Entomology, 17, 288-296. DOI: https://doi.org/10.1111/j.1365-3032.1992.tb01024.x
Vigan, M., 2010. Essential oils: renewal of interest and toxicity. European Journal of Dermatology, 20(6), 685-692.
Villa, J.D., Bustamante, D.M., Dunkley, J.P., Escobar, L.A., 2008. Changes in honey bee (Hymenoptera: Apidae) colony swarming and survival pre- and postarrival of Varroa destructor (Mesostigmata: Varroidae) in Louisiana. Anals of Entomological Society of America, 101 (5), 867-871. DOI: https://doi.org/10.1093/aesa/101.5.867
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). American Bee Journal, 140 (7), 565-572.
Wustenberg, D.G., Grunewald, B., 2004. Pharmacology of the neuronal nicotinic receptor of cultured Kenyon cells of the honeybee, Apis mellifera. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural and Behavioral Physiology, 190, 807-821. DOI: https://doi.org/10.1007/s00359-004-0530-7
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