Effects of octopamine on memory retention under chemical stress: a behavioral study on honey bees

References

• Ahmed, M. A. I., & Vogel, C. F. A. (2020). The synergistic effect of octopamine receptor agonists on selected insect growth regulators on Culex quinquefasciatus Say (Diptera: Culicidae) mosquitoes. One Health, 10(100138), 1–7. https://doi.org/10.1016/j.onehlt.2020.100138
   Google Scholar
• Akülkü, I., Ghanem, S., Suwannapong, G., & Mayack, C. (2021). Age-dependent honey bee appetite regulation is mediated by trehalose and octopamine baseline levels. Insects, 12, 1–12. https://doi.org/10.3390/insects12100863
   Web of Science ®Google Scholar
• Alburaki, M., Steckel, S. J., Chen, D., Mcdermott, E., Weiss, M., Skinner, J. A., Kelly, H., et al. (2017). Landscape and pesticide effects on honey bees: Forager survival and expression of acetylcholinesterase and brain oxidative genes. Apidologie, 48(4), 556–571. https://doi.org/10.1007/s13592-017-0497-3
   Web of Science ®Google Scholar
• Aliouane, Y., El Hassani, A. K., Gary, V., Armengaud, C., Lambin, M., & Gauthier, M. (2009). Subchronic exposure of honey bees to sublethal doses of pesticides: Effects on behavior. Environmental Toxicology and Chemistry, 28(1), 113–122. https://doi.org/10.1897/08-110.1
   PubMed Web of Science ®Google Scholar
• Balfanz, S., Jordan, N., Langenstück, T., Breuer, J., Bergmeier, V., & Baumann, A. (2014). Molecular, pharmacological, and signaling properties of octopamine receptors from honey bee (Apis mellifera) brain. Journal of Neurochemistry, 129(2), 284–296. https://doi.org/10.1111/jnc.12619
   PubMed Web of Science ®Google Scholar
• Barascou, L., Brunet, J. L., Belzunces, L., Decourtye, A., Henry, M., Fourrier, J., Le Conte, Y., & Alaux, C. (2021). Pesticide risk assessment in honey bees: Toward the use of behavioral and reproductive performances as assessment endpoints. Chemosphere, 276(130134), 1–14. https://doi.org/10.1016/j.chemosphere.2021.130134
   Google Scholar
• Barron, A. B., & Robinson, G. E. (2005). Selective modulation of task performance by octopamine in honey bee (Apis mellifera) division of labour. Journal of Comparative Physiology A, 191, 659–668. https://doi.org/10.1007/s00359-005-0619-7
   Web of Science ®Google Scholar
• Barron, A. B., Maleszka, R., Vander Meer, R. K., & Robinson, G. E. (2007). Octopamine modulates honey bee dance behavior. Proceedings of the National Academy of Sciences of the United States of America, 104(5), 1703–1707. https://doi.org/10.1073/pnas.0610506104
   PubMed Web of Science ®Google Scholar
• Behrends, A., & Scheiner, R. (2012). Octopamine improves learning in newly emerged bees but not in old foragers. The Journal of Experimental Biology, 215(Pt 7), 1076–1083. https://doi.org/10.1242/jeb.063297
   PubMed Web of Science ®Google Scholar
• Belzunces, L. P., Tchamitchian, S., & Brunet, J. L. (2012). Neural effects of insecticides in the honey bee. Apidologie, 43, 348–370. https://doi.org/10.1007/s13592-012-0134-0
   Web of Science ®Google Scholar
• Blenau, W., Wilms, J. A., Balfanz, S., & Baumann, A. (2020). AmOctα2R: Functional characterization of a honey bee octopamine receptor inhibiting adenylyl cyclase activity. International Journal of Molecular Sciences, 21(24)9334, 1–19. https://doi.org/10.3390/ijms21249334
   Web of Science ®Google Scholar
• Bloch, G., & Meshi, A. (2007). Influences of octopamine and juvenile hormone on locomotor behavior and period gene expression in the honey bee, Apis mellifera. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 193(2), 181–199. https://doi.org/10.1007/s00359-006-0179-5
   PubMed Web of Science ®Google Scholar
• Bonmatin, J., Moineau, I., Charvet, R., Fleche, C., Colin, M., & Bengsch, E. (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
   PubMed Web of Science ®Google Scholar
• Bonnafé, E., Drouard, F., Hotier, L., Carayon, J. L., Marty, P., Treilhou, M., & Armengaud, C. (2015). Effect of a thymol application on olfactory memory and gene expression levels in the brain of the honey bee Apis mellifera. Environmental Science and Pollution Research, 22(11), 8022–8030. https://doi.org/10.1007/s11356-014-2616-2
   PubMed Web of Science ®Google Scholar
• Brocato, J., & Costa, M. (2013). Basic mechanics of DNA methylation and the unique landscape of the DNA methylome in metal-induced carcinogenesis. Critical Reviews in Toxicology, 43(6), 493–514. https://doi.org/10.3109/10408444.2013.794769
   PubMed Web of Science ®Google Scholar
• Buckemüller, C., Siehler, O., Göbel, J., Zeumer, R., Ölschläger, A., & Eisenhardt, D. (2017). Octopamine underlies the counter-regulatory response to a glucose deficit in honey bees (Apis mellifera). Frontiers in Systems Neuroscience, 11(63), 1–13. https://doi.org/10.3389/fnsys.2017.00063
   PubMedGoogle Scholar
• Burden, C. M., Morgan, M. O., Hladun, K. R., Amdam, G. V., Trumble, J. J., & Smith, B. H. (2019). Acute sublethal exposure to toxic heavy metals alters honey bee (Apis mellifera) feeding behavior. Scientific Reports, 9(4253), 1–10. https://doi.org/10.1038/s41598-019-40396-x
   PubMedGoogle Scholar
• Cabe, S. I. M., Ferro, M. W. B., Farina, W. M., & Hrncir, M. (2017). Dose- and time-dependent effects of oral octopamine treatments on the sucrose responsiveness in stingless bees (Melipona scutellaris). Apidologie, 48, 1–7. https://doi.org/10.1007/s13592-016-0442-x
   Web of Science ®Google Scholar
• Chia, J., & Scott, K. (2020). Activation of specific mushroom body output neurons inhibits proboscis extension and sucrose consumption. PLoS One. 15(1), e0223034. 1-16. https://doi.org/10.1371/journal.pone.0223034
   PubMed Web of Science ®Google Scholar
• Colin, T., Forster, C. C., Westacott, J., Wu, X., Meikle, W. G., & Barron, A. B. (2021). Effects of late miticide treatments on foraging and colony productivity of European honey bees (Apis mellifera). Apidologie, 52(2), 474–492. https://doi.org/10.1007/s13592-020-00837-3
   Web of Science ®Google Scholar
• Colin, T., Plath, J. A., Klein, S., Vine, P., Devaud, J. M., Lihoreau, M., Meikle, W. G., & Barron, A. B. (2020). The miticide thymol in combination with trace levels of the neonicotinoid imidacloprid reduces visual learning performance in honey bees (Apis mellifera). Apidologie, 51, 499–509. https://doi.org/10.1007/s13592-020-00737-6
   Web of Science ®Google Scholar
• Corby-Harris, V., Deeter, M. E., Snyder, L., Meador, C., Welchert, A. C., Hoffman, A., & Obernesser, B. T. (2020). Octopamine mobilizes lipids from honey bee (Apis mellifera) hypopharyngeal glands. Journal of Experimental Biology, 223jeb216135, 1–9. https://doi.org/10.1242/jeb.216135
   Web of Science ®Google Scholar
• Cresswell, J. E., Desneux, N., & van Engelsdorp, D. (2012). Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria. Pest Management Science, 68(6), 819–827. https://doi.org/10.1002/ps.3290
   PubMed Web of Science ®Google Scholar
• de Mattos, I. M., Soares, A. E. E., & Tarpy, D. R. (2018). Mitigating effects of pollen during paraquat exposure on gene expression and pathogen prevalence in Apis mellifera L. Ecotoxicology, 27, 32–44. https://doi.org/10.1007/s10646-017-1868-2
   PubMed Web of Science ®Google Scholar
• Decourtye, A., Armengaud, C., Renou, M., Devillers, J., Cluzeau, S., Gauthier, M., & Pham-Delègue, M. H. (2004). Imidacloprid impairs memory and brain metabolism in the honey bee (Apis mellifera L.). Pesticide Biochemistry and Physiology, 78(2), 83–92. https://doi.org/10.1016/j.pestbp.2003.10.001
   Web of Science ®Google Scholar
• Démares, F. J., Crous, K. L., Pirk, C. W., Nicolson, S. W., & Human, H. (2016). Sucrose sensitivity of honey bees is differently affected by dietary protein and a neonicotinoid pesticide. PLoS One. 11(6)e0156584, 1–16. https://doi.org/10.1371/journal.pone.0223034
   Web of Science ®Google Scholar
• Denker, M., Finke, R., Schaupp, F., Grün, S., & Menzel, R. (2010). Neural correlates of odor learning in the honey bee antennal lobe. European Journal of Neuroscience, 31(1), 119–133. https://doi.org/10.1111/j.1460-9568.2009.07046.x
   PubMed Web of Science ®Google Scholar
• Erber, J., & Kloppenburg, P. (1995). The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.) Journal of Comparative Physiology A, 176, 111–118. https://doi.org/10.1007/BF00197757
   Web of Science ®Google Scholar
• Farooqui, T. (2013). A potential link among biogenic amines-based pesticides, learning and memory, and colony collapse disorder: A unique hypothesis. Neurochemistry International, 62(1), 122–136. https://doi.org/10.1016/j.neuint.2012.09.020
   PubMed Web of Science ®Google Scholar
• Farooqui, T., Robinson, K., Vaessin, H., & Smith, B. H. (2003). Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honey bee. The Journal of Neuroscience, 23(12), 5370–5380. https://doi.org/10.1523/JNEUROSCI.23-12-05370.2003
   PubMed Web of Science ®Google Scholar
• Felsenberg, J., Gehring, K. B., Antemann, V., & Eisenhardt, D. (2011). Behavioural pharmacology in classical conditioning of the proboscis extension response in honey bees (Apis mellifera). Journal of Visualized Experiments, 47(2282), 1–5. https://doi.org/10.3791/2282
   Google Scholar
• Fussnecker, B. L., Smith, B. H., & Mustard, J. A. (2006). Octopamine and tyramine influence the behavioral profile of locomotor activity in the honey bee (Apis mellifera). Journal of Insect Physiology, 52(10), 1083–1092. https://doi.org/10.1016/j.jinsphys.2006.07.008
   PubMed Web of Science ®Google Scholar
• Gashout, H. A., Guzman-Novoab, E., Goodwinb, P. H., & Correa-Benítezc, A. (2020). Impact of sublethal exposure to synthetic and natural acaricides on honey bee (Apis mellifera) memory and expression of genes related to memory. Journal of Insect Physiology, 121(104014), 1–8. https://doi.org/10.1016/j.jinsphys.2020.104014
   Google Scholar
• Giray, T., Galindo-Cardona, A., & Oskay, D. (2007). Octopamine influences honey bee foraging preference. Journal of Insect Physiology, 53(7), 691–698. https://doi.org/10.1016/j.jinsphys.2007.03.016
   PubMed Web of Science ®Google Scholar
• Giurfa, M., & Sandoz, J. C. (2012). Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honey bees. Learning & Memory, 19(2), 54–66. https://doi.org/10.1101/lm.024711.111
   PubMed Web of Science ®Google Scholar
• Glavan, G. (2020). Histochemical staining of acetylcholinesterase in carnolian honey bee (Apis mellifera carnica) brain after chronic exposure to organophosphate diazinon. Journal of Apicaltural Science, 64(1), 123–130. https://doi.org/10.2478/jas-2020-0003
   Web of Science ®Google Scholar
• Gonalons, C. M., & Farina, W. M. (2018). Impaired associative learning after chronic exposure to pesticides in young adult honey bees. Journal of Experimental Biology, 221(7), 1–11. https://doi.org/10.1242/jeb.176644
   Web of Science ®Google Scholar
• Gregorc, A., Alburaki, M., Rinderer, N., Sampson, B., Knight, P. R., Karim, S., & Adamczyk, J. (2018). Effects of coumaphos and imidacloprid on honey bee (Hymenoptera: Apidae) lifespan and antioxidant gene regulations in laboratory experiments. Scientific Reports, 8(15003), 1–13. https://doi.org/10.1038/s41598-018-33348-4
   PubMedGoogle Scholar
• Grohmann, L., Blenau, W., Erber, J., Ebert, P. R., Strünker, T., & Baumann, A. (2003). Molecular and functional characterization of an octopamine receptor from honey bee (Apis mellifera) brain. Journal of Neurochemistry, 86(3), 725–735. https://doi.org/10.1046/j.1471-4159.2003.01876.x
   PubMed Web of Science ®Google Scholar
• Guo, L., Fan, X-y., Qiao, X., Montell, C., Huang, J. (2021). An octopamine receptor confers selective toxicity of amitraz on honey bees and Varroa mites An octopamine receptor confers selective toxicity of amitraz on honey bees and Varroa mites. eLife,10:e68268. https://doi.org/10.7554/eLife.68268
   Google Scholar
• Hammer, M., & Menzel, R. (1998). Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honey bees. Learning & Memory, 5(1), 146–156.
   PubMed Web of Science ®Google Scholar
• He, B., Liu, Z., Wang, Y., Cheng, L., Qing, Q., Duan, J., Xu, J., Dang, X., Zhou, Z., & Li, Z. (2021). Imidacloprid activates ROS and causes mortality in honey bees (Apis mellifera) by inducing iron overload. Ecotoxicology and Environmental Safety, 228(112709) https://doi.org/10.1016/j.ecoenv.2021.112709
   Google Scholar
• Hernández, J., Riveros, A. J., & Amaya-Márquez, M. (2021). Sublethal doses of glyphosate impair olfactory memory retention, but not learning in the honey bee (Apis mellifera scutellata). Journal of Insect Conservation, 25(4), 683–694. https://doi.org/10.1007/s10841-021-00335-6
   Web of Science ®Google Scholar
• Himmelreich, S., & Grünewald, B. (2012). Cellular physiology of olfactory learning in the honey bee brain. Apidologie, 43(3), 308–321. https://doi.org/10.1007/s13592-012-0135-z
   Web of Science ®Google Scholar
• Hoshikawa, H., Uno, M., Honjoh, S., & Nishida, E. (2017). Octopamine enhances oxidative stress resistance through the fasting-responsive transcription factor DAF-16/FOXO in C. elegans. Genes to Cells, 22, 210–219.
   PubMed Web of Science ®Google Scholar
• Iqbal, J., Alqarni, A., & Raweh, H. (2018). Effect of sub-lethal doses of imidacloprid on learning and memory formation of indigenous Arabian bee (Apis mellifera jemenitica Ruttner) adult foragers. Neotropical Entomology, 48, 1–8. https://doi.org/10.1007/s13744-018-0651-2
   PubMed Web of Science ®Google Scholar
• Klein, S., Cabirol, A., Devaud, J. M., Barron, A. B., & Lihoreau, M. (2017). Why bees are so vulnerable to environmental stressors. Trends in Ecology & Evolution, 32(4), 268–278. https://doi.org/10.1146/annurev-ento-011613-162005
   PubMed Web of Science ®Google Scholar
• Lemmon, J. (2010). The effects of β-Sitosterol-β-D-Glucoside (BSSG) and paraquat on sucrose sesensitivityolfactory conditioning and motor development in honey bees, Apis mellifera. A thesis for the degree of Master of Science in Zoology University of Otago.
   Google Scholar
• Li, Z. G., Li, M., Huang, J. N., Ma, C. S., Xiao, L. C., Huang, Q., Zhao, Y. Z., Nie, H. Y., & Su, S. K. (2017). Effects of sublethal concentrations of chlorpyrifos on olfactory learning and memory performances in two bee species, Apis mellifera and Apis cerana. Sociobiology, 64(2), 174–181. https://doi.org/10.13102/sociobiology.v64i2.1385
   Web of Science ®Google Scholar
• Lin, M., Colon-Perez, L. M., Sambo, D. O., Miller, D. R., Lebowitz, J. J., Jimenez-Rondan, F., Cousins, R. J., Horenstein, N., Aydemir, T. B., Febo, M., & Khoshbouei, H. (2020). Mechanism of manganese dysregulation of dopamine neuronal activity. Journal of Neuroscience, 40(30), 5871–5891. https://doi.org/10.1523/JNEUROSCI.2830-19.2020
   PubMed Web of Science ®Google Scholar
• Linn, M., Glaser, S. M., Peng, T., & Grüter, C. (2020). Octopamine and dopamine mediate waggle dance following and information use in honey bees. Proceedings of the Royal Society B, 287(1936)20201950, 1–7. https://doi.org/10.1098/rspb.2020.1950
   Web of Science ®Google Scholar
• Luo, Q. H., Gao, J., Guo, Y., Liu, C., Ma, Y. Z., Zhou, Z. Y., Dai, P. L., Hou, C. S., Wu, Y. Y., & Diao, Q. Y. (2021). Effects of a commercially formulated glyphosate solutions at recommended concentrations on honey bee (Apis mellifera L.) behaviours. Scientific Reports, 11(2115), 1–8. https://doi.org/10.1038/s41598-020-80445-4
   PubMedGoogle Scholar
• Matsumoto, Y., Matsumoto, C. S., Wakuda, R., Ichihara, S., & Mizunami, M. (2015). Roles of octopamine and dopamine in appetitive and aversive memory acquisition studied in olfactory conditioning of maxillary palpi extension response in crickets. Frontiers in Behavioral Neuroscience, 9(230), 1–9. https://doi.org/10.3389/fnbeh.2015.00230
   PubMedGoogle Scholar
• Menzel, R. (2012). The honey bee as a model for understanding the basis of cognition. Nature Reviews Neuroscience, 13, 758–768. https://doi.org/10.1038/nrn3357
   PubMed Web of Science ®Google Scholar
• Menzel, R., & Muller, U. (1996). Learning and memory in honey bees: From behavior to neural substrates. Annual Review of Neuroscience, 19, 379–404. https://doi.org/10.1146/annurev.ne.19.030196.002115
   PubMed Web of Science ®Google Scholar
• Menzel, R., Manz, G., Menzel, R., & Greggers, U. (2001). Massed and spaced learning in honey bees: the role of CS, US, the intertrial interval, and the test interval. Learning & Memory, 8(4), 198–208. https://doi.org/10.1101/lm.40001
   PubMed Web of Science ®Google Scholar
• Mercer, A. R., & Menzel, R. (1982). The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honey bee, Apis mellifera. Journal of Comparative Physiology A, 145, 363–368. https://doi.org/10.1007/BF00619340
   Web of Science ®Google Scholar
• Monchanin, C., Drujont, E., Devaud, J. M., Lihoreau, M., & Barron, A. B. (2021). Heavy metal pollutants have additive negative effects on honey bee cognition. Journal of Experimental Biology, 224(12), 1–7. https://doi.org/10.1242/jeb.241869
   PubMed Web of Science ®Google Scholar
• Mustard, J. A., Gott, A., Scott, J., Chavarria, N. L., & Wright, G. A. (2020). Honey bees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide. Journal of Experimental Biology, 223(5), 1–8. https://doi.org/10.1242/jeb.217174
   Web of Science ®Google Scholar
• Ohta, H., & Ozoe, Y. (2014). Molecular signalling, pharmacology, and physiology of octopamine and tyramine receptors as potential insect pest control targets. Advances in Insect Physiology, 46, 73–166. https://doi.org/10.1016/B978-0-12-417010-0.00002-1
   Web of Science ®Google Scholar
• Pankau, C., & Cooper, R. L. (2022). Molecular physiology of manganese in insects. Current Opinion in Insect Science, 51, 1–7. https://doi.org/10.1016/j.cois.2022.100886
   Web of Science ®Google Scholar
• Pankiw, T., Waddington, K. D., & Page, R. E. (2001). Modulation of sucrose response thresholds in honey bees (Apis mellifera): influence of genotype, feeding and foraging experience. Journal of Comparative Physiology A, 87, 293–301. https://doi.org/10.1007/s003590100201
   Google Scholar
• Peng, T., Schroeder, M., & Grüter, C. (2020). Octopamine increases individual and collective foraging in a neotropical stingless bee. Biology Letters, 16(20200238), 1–5. https://doi.org/10.1098/rsbl.2020.0238
   Google Scholar
• Pham-Delègue, M. H., Jong, R. D., & Masson, C. (1990). Age dependency of the conditioned proboscis extension response in honey bees. Comptes Rendus Des Séances de L'Académie Des Sciences, 310, 527–532.
   Web of Science ®Google Scholar
• Rand, E., Smit, S., Beukes, M., Apostolides, Z., Pirk, C. W., & Nicolson, S. W. (2015). Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine. Scientific Reports, 5(11779), 1–11. https://doi.org/10.1038/srep11779
   Google Scholar
• Raza, M. F., Wang, T., Li, Z., Nie, H., Giurfa, M., Husain, A., Hlavácˇ, P., Kodrik, M., Ali, M. A., Rady, A., & Su, S. (2022). Biogenic amines mediate learning success in appetitive odor conditioning in honey bees. Journal of King Saud University – Science, 34(101928), 1–7. https://doi.org/10.1016/j.jksus.2022.101928
   Google Scholar
• Reim, T., & Scheiner, R. (2014). Division of labour in honey bees: Age- and task-related changes in the expression of octopamine receptor genes. Insect Molecular Biology, 23(6), 833–841. https://doi.org/10.1111/imb.12130
   PubMed Web of Science ®Google Scholar
• Rein, J., Mustard, J., Strauch, M., Smith, B. H., & Galizia, C. G. (2013). Octopamine modulates activity of neural networks in the honey bee antennal lobe. Journal of Comparative Physiology A, 199(11), 947–962. https://doi.org/10.1007/s00359-013-0805-y
   Web of Science ®Google Scholar
• Scheiner, R., Abramson, C. I., Brodschneider, R., Crailsheim, K., Farina, W. M., Fuchs, S., Gruenewald, B., Hahshold, S., Karrer, M., & Koeniger, G. (2013). Standard methods for behavioural studies of Apis mellifera. Journal of Apicaltural Research, 52(4), 1–58. https://doi.org/10.3896/IBRA.1.52.4.04
   Web of Science ®Google Scholar
• Scheiner, R., Baumann, A., & Blenau, W. (2006). Aminergic control and modulation of honey bee behaviour. Current Neuropharmacology, 4(4), 259–276. https://doi.org/10.2174/157015906778520791
   PubMed Web of Science ®Google Scholar
• Scheiner, R., Pluckhahn, S., Oney, B., Blenau, W., & Erber, J. (2002). Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees. Behavioural Brain Research, 136(2), 545–553. https://doi.org/10.1016/S0166-4328(02)00205-X
   PubMed Web of Science ®Google Scholar
• Scheiner, R., Reim, T., Søvik, E., Entler, B. V., Barron, A. B., & Thamm, M. (2017). Learning, gustatory responsiveness and tyramine differences across nurse and forager honey bees. Journal of Experimental Biology, 220(8), 1443–1450. https://doi.org/10.1242/jeb.152496
   PubMed Web of Science ®Google Scholar
• Scheiner, R., Steinbach, A., Classen, G., Strudthoff, N., & Scholz, H. (2014a). Octopamine indirectly affects proboscis extension response habituation in Drosophila melanogaster by controlling sucrose responsiveness. Journal of Insect Physiology, 69, 107–117. https://doi.org/10.1016/j.jinsphys.2014.03.011
   PubMed Web of Science ®Google Scholar
• Scheiner, R., Toteva, A., Reim, T., Søvik, E., & Barron, A. B. (2014b). Differences in the phototaxis of pollen and nectar foraging honey bees are related to their octopamine brain titers. Frontiers in Physiology (Invertebrate Physiology), 116, 1–8. https://doi.org/10.3389/fphys.2014.00116
   PubMedGoogle Scholar
• Schilcher, F., Thamm, M., Strube-Bloss, M., & Scheiner, R. (2021). Opposing actions of octopamine and tyramine on honey bee vision. Biomolecules, 11(9), 1374. https://doi.org/10.3390/biom11091374
   PubMed Web of Science ®Google Scholar
• Schulz, D. J., & Robinson, G. E. (1999). Biogenic amines and division of labor in honey bee colonies: Behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology, 184(5), 481–488. https://doi.org/10.1007/s003590050348
   PubMed Web of Science ®Google Scholar
• Schulz, D. J., & Robinson, G. E. (2001). Octopamine influences division of labor in honey bee colonies. Journal of Comparative Physiology A, 187, 53–61. https://doi.org/10.1007/s003590000177
   PubMed Web of Science ®Google Scholar
• Selcho, M., & Pauls, D. (2019). Linking physiological processes and feeding behaviors by octopamine. Current Opinion in Insect Science, 36, 125–130. https://doi.org/10.1016/j.cois.2019.09.002
   PubMed Web of Science ®Google Scholar
• Senut, M. C., Sen, A., Cingolani, P., Shaik, A., Land, S. J., & Ruden, D. M. (2014). Lead exposure disrupts global DNA methylation in human embryonic stem cells and alters their neuronal differentiation. Toxicological Sciences, 139, 142–161. https://doi.org/10.1093/toxsci/kfu028
   PubMed Web of Science ®Google Scholar
• Siviter, H., Koricheva, J., Brown, M. J. F., & Leadbeater, E. (2018). Quantifying the impact of pesticides on learning and memory in bees. Journal of Applied Ecology, 55(6), 2812–2821. https://doi.org/10.1111/1365-2664.13193
   PubMed Web of Science ®Google Scholar
• Škerl, M. I. S., Bolta, V., Česnik, H. B., & Gregorc, A. (2009). Residues of pesticides in honey bee (Apis mellifera carnica) bee bread and in pollen loads from treated apple orchards. Bulletin of Environmental Contamination and Toxicology, 83, 374–377. https://doi.org/10.1007/s00128-009-9762-0
   PubMed Web of Science ®Google Scholar
• Søvik, E., Perry, C. J., LaMora, A., Barron, A. B., & Ben-Shahar, Y. (2015). Negative impact of manganese on honey bee foraging. Biology Letters, 11(3), 1–4. https://doi.org/10.1098/rsbl.2014.0989
   Web of Science ®Google Scholar
• Stanley, J., Chandrasekaran, C., Preetha, G., & Kuttalam, S. (2010). Toxicity of diafenthiuron to honey bees in laboratory, semi-field and field conditions. Pest Management Science, 66(5), 505–510. https://doi.org/10.1002/ps.1900
   PubMed Web of Science ®Google Scholar
• Tamano, H., & Takeda, A. (2011). Dynamic action of neurometals at the synapse. Metallomics, 3(7), 656–661. https://doi.org/10.1039/c1mt00008j
   PubMed Web of Science ®Google Scholar
• Tian, Y., & Wang, L. (2018). Octopamine mediates protein-seeking behavior in mated female Drosophila. Cell Discovery, 4(66), 1–5. https://doi.org/10.1038/s41421-018-0063-9
   PubMedGoogle Scholar
• Tong, Z., Duan, J., Wu, Y., Liu, Q., He, Q., Shi, Y., Yu, L., & Cao, H. (2018). A survey of multiple pesticide residues in pollen and beebread collected in China. Science of the Total Environment, 640–641, 1578–1586. https://doi.org/10.1016/j.scitotenv.2018.04.424
   Web of Science ®Google Scholar
• Vergoz, V., Roussel, E., Sandoz, J. C., & Giurfa, M. (2007). Aversive learning in honey bees revealed by the olfactory conditioning of the sting extension reflex. PLoS One. 3(e288), 1–10. https://doi.org/10.1371/journal.pone.0000288
   Google Scholar
• Zaidi, A., Fernandes, D., Bean, J. L., & Michaelis, M. L. (2009). Effects of paraquat-induced oxidative stress on the neuronal plasma membrane Ca2+-ATPase. Free Radical Biology and Medicine, 47(10), 1507–1514. https://doi.org/10.1016/j.freeradbiomed.2009.08.018
   PubMed Web of Science ®Google Scholar
• Zhou, C., & Li, X. (2018). Cytotoxicity of chlorpyrifos to human liver hepatocellular carcinoma cells: Effects on mitochondrial membrane potential and intracellular free Ca2. +Toxin Reviews, 37(4), 259–268. https://doi.org/10.1080/15569543.2017.1386686
   Web of Science ®Google Scholar