Pesticides and pollinator brain: How do neonicotinoids affect the central nervous system of bees?

brain central nervous system honey bees neonicotinoids pesticides pollinators

Journal

The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110

Informations de publication

Date de publication:
11 Sep 2024
Historique:
revised: 11 08 2024
received: 03 05 2024
accepted: 29 08 2024
medline: 11 9 2024
pubmed: 11 9 2024
entrez: 11 9 2024
Statut: aheadofprint

Résumé

Neonicotinoids represent over a quarter of the global pesticide market. Research on their environmental impact has revealed their adverse effect on the cognitive functions of pollinators, in particular of bees. Cognitive impairments, mostly revealed by behavioural studies, are the phenotypic expression of an alteration in the underlying neural circuits, a matter deserving greater attention. Here, we reviewed studies on the impact of field-relevant doses of neonicotinoids on the neurophysiology and neurodevelopment of bees. In particular, we focus on their olfactory system as much knowledge has been gained on the different brain areas that participate in odour processing. Recent studies have revealed the detrimental effects of neonicotinoids at multiple levels of the olfactory system, including modulation of odorant-induced activity in olfactory sensory neurons, diminished neural responses in the antennal lobe (the first olfactory processing centre) and abnormal development of the neural connectivity within the mushroom bodies (central neuropils involved in multisensory integration, learning and memory storage, among others). Given the importance of olfactory perception for multiple aspects of bee biology, the reported disruption of the olfactory circuit, which can occur even upon exposure to sublethal doses of neonicotinoids, has severe consequences at both individual and colony levels. Moreover, the effects reported for a multimodal structure such as the mushroom bodies indicate that neonicotinoids' impact translates to other sensory domains. Assessing the impact of field-relevant doses of pesticides on bee neurophysiology is crucial for understanding how neonicotinoids influence their behaviour in ecological contexts and for defining effective and sustainable agricultural practices.

Identifiants

pubmed: 39258341
doi: 10.1111/ejn.16536
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Sorbonne Université
ID : Funding allocated to M. Giurfa
Organisme : Institut Universitaire de France
ID : IUF Chair of M. Giurfa
Organisme : Sorbonne University

Informations de copyright

© 2024 The Author(s). European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

Références

Aguiar, J.M.R.B.V., Cornélio, R., Nocelli, F., Giurfa, M., & Santos Nascimento, F. (2023) Neonicotinoid effects on tropical bees: Imidacloprid impairs innate appetitive responsiveness, learning and memory in the stingless bee Melipona quadrifasciata.
Al Naggar, Y., Estrella‐Maldonado, H., Paxton, R. J., Solís, T., & Quezada‐Euán, J. J. G. (2022). The insecticide imidacloprid decreases nannotrigona stingless bee survival and food consumption and modulates the expression of detoxification and immune‐related genes. Insects, 13, 972. https://doi.org/10.3390/insects13110972
Aliouane, Y., El Hassani, A. K., Gary, V., Armengaud, C., Lambin, M., & Gauthier, M. (2009). Subchronic exposure of honeybees to sublethal doses of pesticides: Effects on behavior. Environmental Toxicology and Chemistry, 28, 113–122. https://doi.org/10.1897/08-110.1
Alkassab, A. T., & Kirchner, W. H. (2016). Impacts of chronic sublethal exposure to clothianidin on winter honeybees. Ecotoxicology, 25, 1000–1010. https://doi.org/10.1007/s10646-016-1657-3
Alkassab, A. T., & Kirchner, W. H. (2018). Assessment of acute sublethal effects of clothianidin on motor function of honeybee workers using video‐tracking analysis. Ecotoxicology and Environmental Safety, 147, 200–205. https://doi.org/10.1016/j.ecoenv.2017.08.047
Andrione, M., Vallortigara, G., Antolini, R., & Haase, A. (2016). Neonicotinoid‐induced impairment of odour coding in the honeybee. Scientific Reports, 6, 38110. https://doi.org/10.1038/srep38110
Armengaud, C., Causse, N., Aït‐Oubah, J., Ginolhac, A., & Gauthier, M. (2000). Functional cytochrome oxidase histochemistry in the honeybee brain. Brain Research, 859, 390–393. https://doi.org/10.1016/S0006-8993(00)02016-3
Aseperi, A. K., Busquets, R., Hooda, P. S., Cheung, P. C. W., & Barker, J. (2020). Behaviour of neonicotinoids in contrasting soils. Journal of Environmental Management, 276, 111329. https://doi.org/10.1016/j.jenvman.2020.111329
Avarguès‐Weber, A., & Giurfa, M. (2013). Conceptual learning by miniature brains. Proceedings of the Royal Society B: Biological Sciences, 280, 20131907. https://doi.org/10.1098/rspb.2013.1907
Avarguès‐Weber, A., Mota, T., & Giurfa, M. (2012). New vistas on honey bee vision. Apidologie, 433(43), 244–268.
Ayestaran, A., Giurfa, M., & de Brito Sanchez, M. G. (2010). Toxic but drank: Gustatory aversive compounds induce post‐ingestional malaise in harnessed honeybees. PLoS ONE, 5, e15000. https://doi.org/10.1371/journal.pone.0015000
Barascou, L., Brunet, J. L., Belzunces, L., Decourtye, A., Henry, M., Fourrier, J., Le Conte, Y., & Alaux, C. (2021). Pesticide risk assessment in honeybees: Toward the use of behavioral and reproductive performances as assessment endpoints. Chemosphere, 276, 130134. https://doi.org/10.1016/j.chemosphere.2021.130134
Barbara, G. S., Grünewald, B., Paute, S., Gauthier, M., & Raymond‐Delpech, V. (2008). Study of nicotinic acetylcholine receptors on cultured antennal lobe neurones from adult honeybee brains. Invertebrate Neuroscience, 8, 19–29. https://doi.org/10.1007/s10158-007-0062-2
Bass, C., Denholm, I., Williamson, M. S., & Nauen, R. (2015). The global status of insect resistance to neonicotinoid insecticides. Pesticide Biochemistry and Physiology, 121, 78–87. https://doi.org/10.1016/j.pestbp.2015.04.004
Begna, T., & Jung, C. (2021). Effects of sequential exposures of sub‐lethal doses of amitraz and thiacloprid on learning and memory of honey bee foragers, Apis mellifera. Journal of Asia‐Pacific Entomology, 24, 77–83. https://doi.org/10.1016/j.aspen.2021.03.012
Belzunces, L. P., Tchamitchian, S., & Brunet, J. L. (2012). (2012) Neural effects of insecticides in the honey bee. Apidologie, 433(43), 348–370. https://doi.org/10.1007/s13592-012-0134-0
Bestea, L., Paoli, M., Arrufat, P., Ronsin, B., Carcaud, J., Sandoz, J.‐C., Velarde, R., Giurfa, M., & de Brito Sanchez, M. G. (2022). The short neuropeptide F regulates appetitive but not aversive responsiveness in a social insect. iScience, 25, 103619. https://doi.org/10.1016/j.isci.2021.103619
Bestea, L., Réjaud, A., Sandoz, J. C., Carcaud, J., Giurfa, M., & de Brito Sanchez, M. G. (2021). Peripheral taste detection in honey bees: What do taste receptors respond to? The European Journal of Neuroscience, 54, 4417–4444. https://doi.org/10.1111/ejn.15265
Bitterman, M. E., Menzel, R., Fietz, A., & Schäfer, S. (1983). Classical conditioning of proboscis extension in honeybees (Apis mellifera). Journal of Comparative Psychology, 97, 107–119. https://doi.org/10.1037/0735-7036.97.2.107
Blacquière, T., Smagghe, G., Van Gestel, C. A. M., & Mommaerts, V. (2012). Neonicotinoids in bees: A review on concentrations, side‐effects and risk assessment. Ecotoxicology, 21, 973–992. https://doi.org/10.1007/s10646-012-0863-x
Bonmatin, J. M., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D. P., Krupke, C., Liess, M., Long, E., Marzaro, M., Mitchell, E. A., Noome, D. A., Simon‐Delso, N., & Tapparo, A. (2015). Environmental fate and exposure; neonicotinoids and fipronil. Environmental Science and Pollution Research, 22, 35–67. https://doi.org/10.1007/s11356-014-3332-7
Bonmatin, J. M., Moineau, I., Charvet, R., Colin, M. E., Fleche, C., & Bengsch, E. R. (2005). Behaviour of imidacloprid in fields. Toxicity for honey bees. In E. Lichtfouse, J. Schwarzbauer, & R. Didier (Eds.), Environmental chemistry: Green chemistry and pollutants in ecosystems (pp. 483–494). Springer. https://doi.org/10.1007/3-540-26531-7_44
Bonmatin, J. M., Moineau, I., Charvet, R., Fleche, C., Colin, M. E., & Bengsch, E. R. (2003). A LC/APCI‐MS/MS method for analysis of imidacloprid in soils, in plants, and in pollens. Analytical Chemistry, 75, 2027–2033. https://doi.org/10.1021/ac020600b
Bortolotti, L., & Costa, C. (2014). Chemical communication in the honey bee society. In C. Mucignat‐Caretta (Ed.), Neurobiology of chemical communication (pp. 147–210). CRC Press/Taylor & Francis.
Bortolotti, L., Montanari, R., Marcelino, J., Mędrzycki, P., Maini, S., Porrini, C., & Superior, E. (2003). Effects of sub‐lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bulletin of Insectology, 56, 63–67.
Botías, 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, 12731–12740. https://doi.org/10.1021/acs.est.5b03459
Breeze, T. D., Bailey, A. P., Balcombe, K. G., & Potts, S. G. (2011). Pollination services in the UK: How important are honeybees? Agriculture, Ecosystems and Environment, 142, 137–143. https://doi.org/10.1016/j.agee.2011.03.020
Brown, L. A., Ihara, M., Buckingham, S. D., Matsuda, K., & Sattelle, D. B. (2006). Neonicotinoid insecticides display partial and super agonist actions on native insect nicotinic acetylcholine receptors. Journal of Neurochemistry, 99, 608–615. https://doi.org/10.1111/j.1471-4159.2006.04084.x
Buatois, A., Pichot, C., Schultheiss, P., Sandoz, J. C., Lazzari, C. R., Chittka, L., Avarguès‐Weber, A., & Giurfa, M. (2017). Associative visual learning by tethered bees in a controlled visual environment. Scientific Reports, 7, 12903. https://doi.org/10.1038/s41598-017-12631-w
Cabirol, A., & Haase, A. (2019). The neurophysiological bases of the impact of neonicotinoid pesticides on the behaviour of honeybees. Insects, 10, 344. https://doi.org/10.3390/insects10100344
Catae, A. F., Roat, T. C., Pratavieira, M., da Silva, R., Menegasso, A., Palma, M. S., & Malaspina, O. (2018). Exposure to a sublethal concentration of imidacloprid and the side effects on target and nontarget organs of Apis mellifera (Hymenoptera, Apidae). Ecotoxicology, 27, 109–121. https://doi.org/10.1007/s10646-017-1874-4
Charreton, M., Decourtye, A., Henry, M., Rodet, G., Sandoz, J. C., Charnet, P., & Collet, C. (2015). A locomotor deficit induced by sublethal doses of pyrethroid and neonicotinoid insecticides in the honeybee Apis mellifera. PLoS ONE, 10, e0144879. https://doi.org/10.1371/journal.pone.0144879
Charvet, R., Katouzian‐Safadi, M., Colin, M. E., Marchand, P. A., & Bonmatin, J. M. (2004). Insecticides systémiques : De nouveaux risques pour les insectes pollinisateurs. Annales Pharmaceutiques Françaises, 62, 29–35. https://doi.org/10.1016/S0003-4509(04)94278-2
Chen, Y. R., Tzeng, D. T. W., & Yang, E. C. (2021). Chronic effects of imidacloprid on honey bee worker development—Molecular pathway perspectives. International Journal of Molecular Sciences, 22, 11835. https://doi.org/10.3390/ijms222111835
Chittka, L., Thomson, J. D., & Waser, N. M. (1999). Flower constancy, insect psychology, and plant evolution. Naturwissenschaften, 86, 361–377. https://doi.org/10.1007/s001140050636
Crall, J. D., Switzer, C. M., Oppenheimer, R. L., Ford Versypt, A. N., Dey, B., Brown, A., Eyster, M., Guerin, C., Pierce, N. E., Combes, S. A., & de Bivort, B. L. (2018). Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science, 362, 683–686. https://doi.org/10.1126/science.aat1598
De Almeida Rossi, C., Roat, T. C., Tavares, D. A., Cintra‐Socolowski, P., & Malaspina, O. (2013). Brain morphophysiology of Africanized bee Apis mellifera exposed to sublethal doses of imidacloprid. Archives of Environmental Contamination and Toxicology, 65, 234–243. https://doi.org/10.1007/s00244-013-9897-1
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 honeybee (Apis mellifera L.). Pesticide Biochemistry and Physiology, 78, 83–92. https://doi.org/10.1016/j.pestbp.2003.10.001
Decourtye, A., & Devillers, J. (2010). Ecotoxicity of neonicotinoid insecticides to bees. Adv. Exp. Med. Biol., 683, 85–95. https://doi.org/10.1007/978-1-4419-6445-8_8
Decourtye, A., Devillers, J., Cluzeau, S., Charreton, M., & Pham‐Delègue, M. H. (2004). Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi‐field and laboratory conditions. Ecotoxicology and Environmental Safety, 57, 410–419. https://doi.org/10.1016/j.ecoenv.2003.08.001
Decourtye, A., Devillers, J., Genecque, E., Le Menach, K., Budzinski, H., Cluzeau, S., & Pham‐Delègue, M. H. (2005). Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Archives of Environmental Contamination and Toxicology, 48, 242–250. https://doi.org/10.1007/s00244-003-0262-7
Decourtye, A., Lacassie, E., & Pham‐Delégue, M. H. (2003). Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Management Science, 59, 269–278. https://doi.org/10.1002/ps.631
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. https://doi.org/10.1016/S0304-3940(01)02400-4
Démares, F. J., Pirk, C. W. W., Nicolson, S. W., & Human, H. (2018). Neonicotinoids decrease sucrose responsiveness of honey bees at first contact. Journal of Insect Physiology, 108, 25–30. https://doi.org/10.1016/j.jinsphys.2018.05.004
DesJardins, N. S., Harrison, J. F., & Smith, B. H. (2023). The effects of anthropogenic toxins on honey bee learning: Research trends and significance. Apidologie, 54, 1–19.
Dupuis, J. P., Gauthier, M., & Raymond‐Delpech, V. (2011). Expression patterns of nicotinic subunits α2, α7, α8, and β1 affect the kinetics and pharmacology of ACh‐induced currents in adult bee olfactory neuropiles. Journal of Neurophysiology, 106, 1604–1613. https://doi.org/10.1152/jn.00126.2011
Easton, A. H., & Goulson, D. (2013). The neonicotinoid insecticide imidacloprid repels pollinating flies and beetles at field‐realistic concentrations. PLoS ONE, 8, e54819. https://doi.org/10.1371/journal.pone.0054819
EFSA. (2013). Conclusion on the peer review of the pesticide risk assessment of the active substance chlorantraniliprole. EFSA Journal, 11, 3143. https://doi.org/10.2903/j.efsa.2013.3143
EFSA. (2018). Peer review of the pesticide risk assessment for bees for the active substance imidacloprid considering the uses as seed treatments and granules. EFSA Journal, 16, e05178.
El Hassani, A. K., Dacher, M., Gary, V., Lambin, M., Gauthier, M., & Armengaud, C. (2008). Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Archives of Environmental Contamination and Toxicology, 54, 653–661. https://doi.org/10.1007/s00244-007-9071-8
Favaro, R., Roved, J., Haase, A., & Angeli, S. (2022). Impact of chronic exposure to two neonicotinoids on honey bee antennal responses to flower volatiles and pheromonal compounds. Frontiers in Insect Science, 2, 821145. https://doi.org/10.3389/finsc.2022.821145
Fischer, J., Müller, T., Spatz, A. K., Greggers, U., Grünewald, B., & Menzel, R. (2014). Neonicotinoids interfere with specific components of navigation in honeybees. PLoS ONE, 9, e91364. https://doi.org/10.1371/journal.pone.0091364
Francis, R. M., Nielsen, S. L., & Kryger, P. (2013). Varroa‐virus interaction in collapsing honey bee colonies. PLoS ONE, 8, e57540. https://doi.org/10.1371/journal.pone.0057540
Galizia, C. G., Sachse, S., Rappert, A., & Menzel, R. (1999). The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nature Neuroscience, 2, 473–478. https://doi.org/10.1038/8144
Girolami, V., Marzaro, M., Vivan, L., Mazzon, L., Greatti, M., Giorio, C., Marton, D., & Tapparo, A. (2012). Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implication. Journal of Applied Entomology, 136, 17–26. https://doi.org/10.1111/j.1439-0418.2011.01648.x
Giurfa, M. (2007). Behavioral and neural analysis of associative learning in the honeybee: A taste from the magic well. Journal of Comparative Physiology. A, 193, 801–824. https://doi.org/10.1007/s00359-007-0235-9
Giurfa, M., & Núñez, J. A. (1992). Honeybees mark with scent and reject recently visited flowers. Oecologia, 89, 113–117. https://doi.org/10.1007/BF00319022
Giurfa, M., & Sandoz, J.‐C. (2012). Invertebrate learning and memory: Fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learning & Memory, 19, 54–66. https://doi.org/10.1101/lm.024711.111
Giurfa, M., Zhang, S., Jenett, A., Menzel, R., & Srinivasan, M. V. (2001). The concepts of “sameness” and “difference” in an insect. Nature, 410, 930–933. https://doi.org/10.1038/35073582
Graham, K. Z., & Fafinski, M. J. (2019). Federal regulation of pesticide residues: A brief history and analysis. Journal of Food Law & Policy, 15, 1–35.
Groh, C., & Rössler, W. (2011). Comparison of microglomerular structures in the mushroom body calyx of neopteran insects. Arthropod Structure & Development, 40, 358–367. https://doi.org/10.1016/j.asd.2010.12.002
Grünewald, B. (1999). Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera. The Journal of Comparative Neurology, 404, 114–126. https://doi.org/10.1002/(SICI)1096-9861(19990201)404:1<114::AID-CNE9>3.0.CO;2-#
Grünewald, B., & Siefert, P. (2019). Acetylcholine and its receptors in honeybees: Involvement in development and impairments by neonicotinoids. Insects, 10, 420. https://doi.org/10.3390/insects10120420
Guerrieri, F., Schubert, M., Sandoz, J. C., & Giurfa, M. (2005). Perceptual and neural olfactory similarity in honeybees. PLoS Biology, 3, e60. https://doi.org/10.1371/journal.pbio.0030060
Han, P., Niu, C. Y., Lei, C. L., Cui, J. J., & Desneux, N. (2010). Use of an innovative T‐tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera L. Ecotoxicology, 19, 1612–1619. https://doi.org/10.1007/s10646-010-0546-4
Henry, M., Béguin, M., Requier, F., Rollin, O., Odoux, J. F., Aupinel, P., Aptel, J., Tchamitchian, S., & Decourtye, A. (2012). A common pesticide decreases foraging success and survival in honey bees. Science, 336, 348–350. https://doi.org/10.1126/science.1215039
Henry, M., Cerrutti, N., Aupinel, P., Decourtye, A., Gayrard, M., Odoux, J.‐F., Pissard, A., Rüger, C., & Bretagnolle, V. (2015). Reconciling laboratory and field assessments of neonicotinoid toxicity to honeybees. Proceedings of the Royal Society B: Biological Sciences, 282, 20152110. https://doi.org/10.1098/rspb.2015.2110
Hesselbach, H., & Scheiner, R. (2019). The novel pesticide flupyradifurone (Sivanto) affects honeybee motor abilities. Ecotoxicology, 28, 354–366. https://doi.org/10.1007/s10646-019-02028-y
Honkanen, A., Adden, A., Da Silva Freitas, J., & Heinze, S. (2019). The insect central complex and the neural basis of navigational strategies. The Journal of Experimental Biology, 222, jeb188854. https://doi.org/10.1242/jeb.188854
Hourcade, B., Muenz, T. S., Sandoz, J.‐C., Rössler, W., & Devaud, J.‐M. (2010). Long‐term memory leads to synaptic reorganization in the mushroom bodies: A memory trace in the insect brain? The Journal of Neuroscience, 30, 6461–6465. https://doi.org/10.1523/JNEUROSCI.0841-10.2010
Huang, J., Zhang, Z., Feng, W., Zhao, Y., Aldanondo, A., de Brito Sanchez, M. G., Paoli, M., Rolland, A., Li, Z., Nie, H., Lin, Y., Zhang, S., Giurfa, M., & Su, S. (2022). Food wanting is mediated by transient activation of dopaminergic signaling in the honey bee brain. Science, 376, 508–512. https://doi.org/10.1126/science.abn9920
Iqbal, J., Alqarni, A. S., & Raweh, H. S. A. (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, 373–380. https://doi.org/10.1007/s13744-018-0651-2
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, 371–378. https://doi.org/10.1016/j.cropro.2003.08.018
Jeschke, P., Nauen, R., Schindler, M., & Elbert, A. (2011). Overview of the status and global strategy for neonicotinoids. Journal of Agricultural and Food Chemistry, 59, 2897–2908. https://doi.org/10.1021/jf101303g
Jin, N., Klein, S., Leimig, F., Bischoff, G., & Menzel, R. (2015). The neonicotinoid clothianidin interferes with navigation of the solitary bee Osmia cornuta in a laboratory test. The Journal of Experimental Biology, 218, 2821–2825. https://doi.org/10.1242/jeb.123612
Joerges, J., Küttner, A., Galizia, C. G., & Menzel, R. (1997). Representations of odours and odour mixtures visualized in the honeybee brain. Nature, 387, 285–288. https://doi.org/10.1038/387285a0
Kaiser, A., Hensgen, R., Tschirner, K., Beetz, E., Wüstenberg, H., Pfaff, M., Mota, T., & Pfeiffer, K. (2022). A three‐dimensional atlas of the honeybee central complex, associated neuropils and peptidergic layers of the central body. The Journal of Comparative Neurology, 530, 2416–2438. https://doi.org/10.1002/cne.25339
Karahan, A., Çakmak, I., Hranitz, J. M., Karaca, I., & Wells, H. (2015). Sublethal imidacloprid effects on honey bee flower choices when foraging. Ecotoxicology, 24, 2017–2025. https://doi.org/10.1007/s10646-015-1537-2
Ke, L., Chen, X., Dai, P., & Liu, Y. J. (2023). Chronic larval exposure to thiacloprid impairs honeybee antennal selectivity, learning and memory performances. Frontiers in Physiology, 14, 1114488. https://doi.org/10.3389/fphys.2023.1114488
Kessler, S. C., Tiedeken, E. J., Simcock, K. L., Derveau, S., Mitchell, J., Softley, S., Stout, J. C., & Wright, G. A. (2015). Bees prefer foods containing neonicotinoid pesticides. Nature, 521, 74–76.
Khalifa, S. A. M., Elshafiey, E. H., Shetaia, A. A., El‐Wahed, A. A. A., Algethami, F. A., Musharraf, S. G., AlAjmi, M. F., Zhao, C., Masry, S. H. D., Abdel‐Daim, M. M., Halabi, M. F., Kai, G., Al Naggar, Y., Bishr, M., Diab, M. A. M., & El‐Seedi, H. R. (2021). Overview of bee pollination and its economic value for crop production. Insects, 12, 688. https://doi.org/10.3390/insects12080688
Kheradmand, B., & Nieh, J. C. (2019). The role of landscapes and landmarks in bee navigation: A review. Insects, 10, 342. https://doi.org/10.3390/insects10100342
Kim, S., Cho, S., & Lee, S. H. (2022). Synergistic effects of imidacloprid and high temperature on honey bee colonies. Apidologie, 53, 67. https://doi.org/10.1007/s13592-022-00980-z
Klein, A.‐M., Vaissière, B. E., Cane, J. H., Steffan‐Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274, 303–313.
Klingelhöfer, D., Braun, M., Brüggmann, D., & Groneberg, D. A. (2022). Neonicotinoids: A critical assessment of the global research landscape of the most extensively used insecticide. Environmental Research, 213, 113727. https://doi.org/10.1016/j.envres.2022.113727
Kozii, I. V., Barnsley, S., Silva, M., Wood, S. C., Klein, C. D., de Mattos, I. M., Zabrodski, M. W., Silva, R. C. M., Fabela, C. I. O., Guillemin, L., Dvylyuk, I., Ferrari, M. C. O., & Simko, E. (2021). Reproductive fitness of honey bee queens exposed to thiamethoxam during development. Veterinary Pathology, 58, 1107–1118. https://doi.org/10.1177/03009858211031845
Kreissl, S., & Bicker, G. (1989). Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor‐like antigen in the brain of the honeybee. The Journal of Comparative Neurology, 286, 71–84. https://doi.org/10.1002/cne.902860105
Krupke, C. H., Hunt, G. J., Eitzer, B. D., Andino, G., & Given, K. (2012). Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE, 7, e29268. https://doi.org/10.1371/journal.pone.0029268
Lafon, G., Paoli, M., Paffhausen, B. H., Sanchez, G. D. B., Lihoreau, M., Avarguès‐weber, A., & Giurfa, M. (2023). Efficient visual learning by bumble bees in virtual‐reality conditions: Size does not matter. Insect Sci., 0, 1–15. https://doi.org/10.1111/1744-7917.13181
Lamberth, C., Jeanmart, S., Luksch, T., & Plant, A. (2013). Current challenges and trends in the discovery of agrochemicals. Science, 341, 742–746. https://doi.org/10.1126/science.1237227
Laurent, F. M., & Rathahao, E. (2003). Distribution of [(14)C]imidacloprid in sunflowers (Helianthus annuus L.) following seed treatment. Journal of Agricultural and Food Chemistry, 51, 8005–8010. https://doi.org/10.1021/jf034310n
Laurino, D., Porporato, M., Patetta, A., & Manino, A. (2011). Toxicity of neonicotinoid insecticides to honey bees: Laboratory tests. Bulletin of Insectology, 64, 107–113.
Le Conte, Y., Ellis, M., & Ritter, W. (2010). Varroa mites and honey bee health: Can Varroa explain part of the colony losses? Apidologie, 41, 353–363. https://doi.org/10.1051/apido/2010017
Li, H., Wu, F., Zhao, L., Tan, J., Jiang, H., & Hu, F. (2015). Neonicotinoid insecticide interact with honeybee odorant‐binding protein: Implication for olfactory dysfunction. International Journal of Biological Macromolecules, 81, 624–630. https://doi.org/10.1016/j.ijbiomac.2015.08.055
Li, Z., Yu, T., Chen, Y., Heerman, M., He, J., Huang, J., Nie, H., & Su, S. (2019). Brain transcriptome of honey bees (Apis mellifera) exhibiting impaired olfactory learning induced by a sublethal dose of imidacloprid. Pesticide Biochemistry and Physiology, 156, 36–43. https://doi.org/10.1016/j.pestbp.2019.02.001
Locatelli, F. F., Fernandez, P. C., & Smith, B. H. (2016). Learning about natural variation of odor mixtures enhances categorization in early olfactory processing. The Journal of Experimental Biology, 219, 2752–2762. https://doi.org/10.1242/jeb.141465
Lu, C., Hung, Y. T., & Cheng, Q. (2020). A review of sub‐lethal neonicotinoid insecticides exposure and effects on pollinators. Current Pollution Reports, 6, 137–151. https://doi.org/10.1007/s40726-020-00142-8
Lu, C., Warchol, K. M., & Callahan, R. A. (2014). Sub‐lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder. Bulletin of Insectology, 67, 125–130.
Lundin, O., Rundlöf, M., Smith, H. G., Fries, I., & Bommarco, R. (2015). Neonicotinoid insecticides and their impacts on bees: A systematic review of research approaches and identification of knowledge gaps. PLoS ONE, 10, e0136928. https://doi.org/10.1371/journal.pone.0136928
Main, A. R., Webb, E. B., Goyne, K. W., Abney, R., & Mengel, D. (2021). Impacts of neonicotinoid seed treatments on the wild bee community in agricultural field margins. Science of the Total Environment, 786, 147299. https://doi.org/10.1016/j.scitotenv.2021.147299
Matsumoto, T. (2013). Reduction in homing flights in the honey bee Apis mellifera after a sublethal dose of neonicotinoid insecticides. Bulletin of Insectology, 66, 1–9.
Mengoni‐Goñalons, C., Alons, G., & Farina, W. M. (2018). Impaired associative learning after chronic exposure to pesticides in young adult honey bees. The Journal of Experimental Biology, 221, jeb176644. https://doi.org/10.1242/jeb.176644
Mengoni‐Goñalons, C., & Farina, W. M. (2015). Effects of sublethal doses of imidacloprid on young adult honeybee behaviour. PLoS ONE, 10, e0140814. https://doi.org/10.1371/journal.pone.0140814
Menzel, R. (1999). Memory dynamics in the honeybee. Journal of Comparative Physiology a, 185, 323–340. https://doi.org/10.1007/s003590050392
Menzel, R. (2012). The honeybee as a model for understanding the basis of cognition. Nature Reviews. Neuroscience, 13, 758–768. https://doi.org/10.1038/nrn3357
Menzel, R. (2014). The insect mushroom body, an experience‐dependent recoding device. Journal of Physiology, Paris, 108, 84–95. https://doi.org/10.1016/j.jphysparis.2014.07.004
Mitchell, E. A. D., Mulhauser, B., Mulot, M., Mutabazi, A., Glauser, G., & Aebi, A. (2017). A worldwide survey of neonicotinoids in honey. Science, 358, 109–111. https://doi.org/10.1126/science.aan3684
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 B: Biological Sciences, 298, 309–354.
Moffat, C., Buckland, S. T., Samson, A. J., McArthur, R., Chamosa Pino, V., Bollan, K. A., Huang, J. T. J., & Connolly, C. N. (2016). Neonicotinoids target distinct nicotinic acetylcholine receptors and neurons, leading to differential risks to bumblebees. Scientific Reports, 6, 24764. https://doi.org/10.1038/srep24764
Mota, T., Gronenberg, W., Giurfa, M., & Sandoz, J.‐C. (2013). Chromatic processing in the anterior optic tubercle of the honey bee brain. The Journal of Neuroscience, 33, 4–16. https://doi.org/10.1523/JNEUROSCI.1412-12.2013
Mullin, C. A., Frazier, M., Frazier, J. L., Ashcraft, S., Simonds, R., Vanengelsdorp, D., & Pettis, J. S. (2010). High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health. PLoS, 5, e9754. https://doi.org/10.1371/journal.pone.0009754
Mustard, J. A., Gott, A., Scott, J., Chavarria, N. L., & Wright, G. A. (2020). Honeybees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide. The Journal of Experimental Biology, 223, jeb217174. https://doi.org/10.1242/jeb.217174
Muth, F., & Leonard, A. S. (2019). A neonicotinoid pesticide impairs foraging, but not learning, in free‐flying bumblebees. Scientific Reports, 9, 4764. https://doi.org/10.1038/s41598-019-39701-5
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. https://doi.org/10.1002/ps.331
Orčić, S. M., Čelić, T. V., Purać, J. S., Vukašinović, E. L., & Kojić, D. K. (2022). Acute toxicity of sublethal concentrations of thiacloprid and clothianidin to immune response and oxidative status of honey bees. Apidologie, 53, 50. https://doi.org/10.1007/s13592-022-00959-w
O'Shea‐Wheller, T. A., Rinkevich, F. D., Danka, R. G., Simone‐Finstrom, M., Tokarz, P. G., & Healy, K. B. (2022). A derived honey bee stock confers resistance to Varroa destructor and associated viral transmission. Scientific Reports, 12, 4852. https://doi.org/10.1038/s41598-022-08643-w
Palmer, M. J., Moffat, C., Saranzewa, N., Harvey, J., Wright, G. A., & Connolly, C. N. (2013). (2013) Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nature Communications, 41(4), 1634. https://doi.org/10.1038/ncomms2648
Paoli, M., & Galizia, G. C. (2021). Olfactory coding in honeybees. Cell and Tissue Research, 383, 35–58. https://doi.org/10.1007/s00441-020-03385-5
Paoli, M., Wystrach, A., Ronsin, B., & Giurfa, M. (2024). Smell and aftersmell: Fast calcium imaging dynamics of honey bee olfactory coding. eLife, 13, RP93789. https://doi.org/10.7554/eLife.93789.3
Parkinson, R. H., Scott, J., Dorling, A. L., Jones, H., Haslam, M., McDermott‐Roberts, A. E., & Wright, G. A. (2023). Mouthparts of the bumblebee (Bombus terrestris) exhibit poor acuity for the detection of pesticides in nectar. eLife, 12, RP89129. https://doi.org/10.7554/eLife.89129
Pelosi, C., Bertrand, C., Daniele, G., Coeurdassier, M., Benoit, P., Nélieu, S., Lafay, F., Bretagnolle, V., Gaba, S., Vulliet, E., & Fritsch, C. (2021). Residues of currently used pesticides in soils and earthworms: A silent threat? Ecosystems & Environment, 305, 107167. https://doi.org/10.1016/j.agee.2020.107167
Peng, Y. C., & Yang, E. C. (2016). Sublethal dosage of imidacloprid reduces the microglomerular density of honey bee mushroom bodies. Scientific Reports, 6, 19298. https://doi.org/10.1038/srep19298
Peng, Y. C., & Yang, E. C. (2017). Reply to ‘pitfalls of using confocal‐microscopy based automated quantification of synaptic complexes in honeybee mushroom bodies (response to Peng and Yang 2016)’. Scientific Reports, 71(7), 11286. https://doi.org/10.1038/s41598-017-11858-x
Pfeiffer, K., & Homberg, U. (2014). Organization and functional roles of the central complex in the insect brain. Annual Review of Entomology, 59, 165–184. https://doi.org/10.1146/annurev-ento-011613-162031
Phillips McDougall/Agribusiness Intelligence. (2018) Evolution of the Crop Protection Industry since 1960.
Piiroinen, S., & Goulson, D. (2016). Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees. Proceedings of the Royal Society B: Biological Sciences, 283, 20160246. https://doi.org/10.1098/rspb.2016.0246
Pilling, E., Campbell, P., Coulson, M., Ruddle, N., & Tornier, I. (2013). A four‐year field program investigating long‐term effects of repeated exposure of honey bee colonies to flowering crops treated with Thiamethoxam. PLoS ONE, 8, e77193. https://doi.org/10.1371/journal.pone.0077193
Rabhi, K. K., Deisig, N., Demondion, E., Le Corre, J., Robert, G., Tricoire‐Leignel, H., Lucas, P., Gadenne, C., & Anton, S. (2016). Low doses of a neonicotinoid insecticide modify pheromone response thresholds of central but not peripheral olfactory neurons in a pest insect. Proceedings of the Royal Society B, 283, 20152987. https://doi.org/10.1098/rspb.2015.2987
Requier, F., Rome, Q., Chiron, G., Decante, D., Marion, S., Menard, M., Muller, F., Villemant, C., & Henry, M. (2019). Predation of the invasive Asian hornet affects foraging activity and survival probability of honey bees in Western Europe. Journal of Pest Science, 92, 567–578. https://doi.org/10.1007/s10340-018-1063-0
Retschnig, G., Rich, J., Crailsheim, K., Pfister, J., Perreten, V., & Neumann, P. (2021). You are what you eat: Relative importance of diet, gut microbiota and nestmates for honey bee, Apis mellifera, worker health. Apidologie, 52, 632–646. https://doi.org/10.1007/s13592-021-00851-z
Rortais, A., Arnold, G., Halm, M. P., & 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, 71–83. https://doi.org/10.1051/apido:2004071
Rossel, S. (1993). Navigation by bees using polarized skylight. Comparative Biochemistry and Physiology, 104A, 695–708. https://doi.org/10.1016/0300-9629(93)90146-U
Rössler, W., Spaethe, J., & Groh, C. (2017). Pitfalls of using confocal‐microscopy based automated quantification of synaptic complexes in honeybee mushroom bodies (response to Peng and Yang 2016). Scientific Reports, 7, 9786. https://doi.org/10.1038/s41598-017-09967-8
Roussel, E., Carcaud, J., Combe, M., Giurfa, M., & Sandoz, J. C. (2014). Olfactory coding in the honeybee lateral horn. Current Biology, 24, 561–567. https://doi.org/10.1016/j.cub.2014.01.063
Rybak, J., & Menzel, R. (1993). Anatomy of the mushroom bodies in the honey bee brain: The neuronal connections of the alpha‐lobe. The Journal of Comparative Neurology, 334, 444–465. https://doi.org/10.1002/cne.903340309
Sachse, S., Rappert, A., & Galizia, C. G. (1999). The spatial representation of chemical structures in the antennal lobe of honeybees: Steps towards the olfactory code. The European Journal of Neuroscience, 11, 3970–3982. https://doi.org/10.1046/j.1460-9568.1999.00826.x
Sandstrom, M. W., Nowell, L. H., Mahler, B. J., & Van Metre, P. C. (2022). New‐generation pesticides are prevalent in California's Central Coast streams. Sci. Total Environ., 806, 150683. https://doi.org/10.1016/j.scitotenv.2021.150683
Sayre, M. E., Templin, R., Chavez, J., Kempenaers, J., & Heinze, S. (2021). A projectome of the bumblebee central complex. eLife, 10, e68911. https://doi.org/10.7554/eLife.68911
Schmuck, R., Schning, 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, 225–238. https://doi.org/10.1002/ps.270
Singla, A., Barmota, H., Kumar Sahoo, S., & Kaur Kang, B. (2021). Influence of neonicotinoids on pollinators: A review. Journal of Apicultural Research, 60, 19–32. https://doi.org/10.1080/00218839.2020.1825044
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, 2812–2821. https://doi.org/10.1111/1365-2664.13193
Stanley, D. A., Russell, A. L., Morrison, S. J., Rogers, C., & Raine, N. E. (2016). Investigating the impacts of field‐realistic exposure to a neonicotinoid pesticide on bumblebee foraging, homing ability and colony growth. Journal of Applied Ecology, 53, 1440–1449. https://doi.org/10.1111/1365-2664.12689
Stanley, D. A., Smith, K. E., & Raine, N. E. (2015). Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide. Scientific Reports, 5, 16508. https://doi.org/10.1038/srep16508
Stark, J. D., Jepson, P. C., & Mayer, D. F. (1995). Limitations to use of topical toxicity data for predictions of pesticide side effects in the field. Journal of Economic Entomology, 88, 1081–1088. https://doi.org/10.1093/jee/88.5.1081
Stoner, K. A., & Eitzer, B. D. (2012). Movement of soil‐applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS ONE, 7, e39114. https://doi.org/10.1371/journal.pone.0039114
Stopfer, M. (2014). Central processing in the mushroom bodies. Current Opinion in Insect Science, 6, 99–103. https://doi.org/10.1016/j.cois.2014.10.009
Stout, J. C., & Goulson, D. (2001). The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Animal Behaviour, 62, 183–189. https://doi.org/10.1006/anbe.2001.1729
Straub, L., Villamar‐Bouza, L., Bruckner, S., Chantawannakul, P., Kolari, E., Maitip, J., Vidondo, B., Neumann, P., & Williams, G. R. (2021). Negative effects of neonicotinoids on male honeybee survival, behaviour and physiology in the field. Journal of Applied Ecology, 58, 2515–2528. https://doi.org/10.1111/1365-2664.14000
Strausfeld, N. J. (2002). Organization of the honey bee mushroom body: Representation of the calyx within the vertical and gamma lobes. The Journal of Comparative Neurology, 450, 4–33. https://doi.org/10.1002/cne.10285
Suchet, C., Dormont, L., Schatz, B., Giurfa, M., Simon, V., Raynaud, C., & Chave, J. (2011). Floral scent variation in two Antirrhinum majus subspecies influences the choice of naïve bumblebees. Behavioral Ecology and Sociobiology, 65, 1015–1027.
Taillebois, E., Cartereau, A., Jones, A. K., & Thany, S. H. (2018). Neonicotinoid insecticides mode of action on insect nicotinic acetylcholine receptors using binding studies. Pesticide Biochemistry and Physiology, 151, 59–66. https://doi.org/10.1016/j.pestbp.2018.04.007
Takeda, K. (1961). Classical conditioned response in the honey bee. Journal of Insect Physiology, 6, 168–179. https://doi.org/10.1016/0022-1910(61)90060-9
Tantillo, G., Bottaro, M., Di Pinto, A., Martella, V., Di Pinto, P., & Terio, V. (2015). Virus infections of honeybees Apis mellifera. Italian Journal of Food Safety, 4, 5364. https://doi.org/10.4081/ijfs.2015.5364
Tavares, D. A., Roat, T. C., Carvalho, S. M., Silva‐Zacarin, E. C. M., & Malaspina, O. (2015). In vitro effects of thiamethoxam on larvae of Africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere, 135, 370–378. https://doi.org/10.1016/j.chemosphere.2015.04.090
Tavares, D. A., Roat, T. C., Silva‐Zacarin, E. C. M., Nocelli, R. C. F., & Malaspina, O. (2019). Exposure to thiamethoxam during the larval phase affects synapsin levels in the brain of the honey bee. Ecotoxicology and Environmental Safety, 169, 523–528. https://doi.org/10.1016/j.ecoenv.2018.11.048
Thany, S. H. (2023). Molecular mechanism of action of neonicotinoid insecticides. International Journal of Molecular Sciences, 24, 5484.
Thany, S. H., Crozatier, M., Raymond‐Delpech, V., Gauthier, M., & Lenaers, G. (2005). Apisalpha2, Apisalpha7‐1 and Apisalpha7‐2: Three new neuronal nicotinic acetylcholine receptor alpha‐subunits in the honeybee brain. Gene, 344, 125–132. https://doi.org/10.1016/j.gene.2004.09.010
Thompson, H. M., Wilkins, S., Harkin, S., Milner, S., & Walters, K. F. A. (2015). Neonicotinoids and bumblebees (Bombus terrestris): Effects on nectar consumption in individual workers. Pest Management Science, 71, 946–950. https://doi.org/10.1002/ps.3868
Tison, L., Hahn, M. L., Holtz, S., Rossner, A., Greggers, U., Bischoff, G., & Menzel, R. (2016). Honey bees' behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field. Environmental Science & Technology, 50, 7218–7227. https://doi.org/10.1021/acs.est.6b02658
Tison, L., Rößner, A., Gerschewski, S., & Menzel, R. (2019). The neonicotinoid clothianidin impairs memory processing in honey bees. Ecotoxicology and Environmental Safety, 180, 139–145. https://doi.org/10.1016/j.ecoenv.2019.05.007
Tomé, H. V. V., Martins, G. F., Lima, M. A. P., Campos, L. A. O., & Guedes, R. N. C. (2012). Imidacloprid‐induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS ONE, 7, e38406. https://doi.org/10.1371/journal.pone.0038406
Tosi, S., Burgio, G., & Nieh, J. C. (2017). A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Scientific Reports, 7, 1201. https://doi.org/10.1038/s41598-017-01361-8
Tosi, S., Demares, F. J., Nicolson, S. W., Medrzycki, P., Pirk, C. W., & Human, H. (2016). Effects of a neonicotinoid pesticide on thermoregulation of African honey bees (Apis mellifera scutellata). Journal of Insect Physiology, 93‐94, 56–63. https://doi.org/10.1016/j.jinsphys.2016.08.010
Tosi, S., & Nieh, J. C. (2017). A common neonicotinoid pesticide, thiamethoxam, alters honey bee activity, motor functions, and movement to light. Scientific Reports, 7, 15132. https://doi.org/10.1038/s41598-017-15308-6
UNEP. (2021) Status and trends of pesticide use, Environmental and Health Impacts of Pesticides and Fertilizers and Ways of Minimizing Them.
Villar, M. E., Marchal, P., Viola, H., & Giurfa, M. (2020). Redefining single‐trial memories in the honeybee. Cell Reports, 30, 2603–2613. https://doi.org/10.1016/j.celrep.2020.01.086
Wagner, D. L., Grames, E. M., Forister, M. L., Berenbaum, M. R., & Stopak, D. (2021). Insect decline in the Anthropocene: Death by a thousand cuts. Proceedings of the National Academy of Sciences of the United States of America, 118, e2023989118. https://doi.org/10.1073/pnas.2023989118
Warner, S., Pokhrel, L. R., Akula, S. M., Ubah, C. S., Richards, S. L., Jensen, H., & Kearney, G. D. (2024). A scoping review on the effects of Varroa mite (Varroa destructor) on global honey bee decline. Science of the Total Environment, 906, 167492. https://doi.org/10.1016/j.scitotenv.2023.167492
Waser, N. M. (1986). Flower constancy: Definition, cause, and measurement. The American Naturalist, 127, 593–603. https://doi.org/10.1086/284507
Williamson, S. M., Willis, S. J., & Wright, G. A. (2014). Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology, 23, 1409–1418. https://doi.org/10.1007/s10646-014-1283-x
Williamson, S. M., & Wright, G. A. (2013). Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. The Journal of Experimental Biology, 216, 1799–1807. https://doi.org/10.1242/jeb.083931
Willis Chan, D. S., & Raine, N. E. (2021). Population decline in a ground‐nesting solitary squash bee (Eucera pruinosa) following exposure to a neonicotinoid insecticide treated crop (Cucurbita pepo). Scientific Reports, 11, 4241. https://doi.org/10.1038/s41598-021-83341-7
Wood, T. J., Kaplan, I., Zhang, Y., & Szendrei, Z. (2019). Honeybee dietary neonicotinoid exposure is associated with pollen collection from agricultural weeds. Proceedings of the Royal Society B, 286, 20190989. https://doi.org/10.1098/rspb.2019.0989
Wright, G. A., & Schiestl, F. P. (2009). The evolution of floral scent: The influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Functional Ecology, 23, 841–851. https://doi.org/10.1111/j.1365-2435.2009.01627.x
Wright, G. A., & Smith, B. H. (2004). Different thresholds for detection and discrimination of odors in the honey bee (Apis mellifera). Chemical Senses, 29, 127–135. https://doi.org/10.1093/chemse/bjh016
Wright, G. A., Softley, S., & Earnshaw, H. (2015). Low doses of neonicotinoid pesticides in food rewards impair short‐term olfactory memory in foraging‐age honeybees. Scientific Reports, 5, 15322. https://doi.org/10.1038/srep15322
Yao, J., Zhu, Y. C., & Adamczyk, J. (2018). Responses of honey bees to lethal and sublethal doses of formulated clothianidin alone and mixtures. Journal of Economic Entomology, 111, 1517–1525. https://doi.org/10.1093/jee/toy140
Yu, X., Wang, M., Kang, M., Liu, L., Guo, X., & Xu, B. (2011). Molecular cloning and characterization of two nicotinic acetylcholine receptor β subunit genes from Apis cerana cerana. Archives of Insect Biochemistry and Physiology, 77, 163–178. https://doi.org/10.1002/arch.20432
Zhang, E., & Nieh, J. C. (2015). The neonicotinoid imidacloprid impairs honey bee aversive learning of simulated predation. The Journal of Experimental Biology, 218, 3199–3205. https://doi.org/10.1242/jeb.127472
Zhu, Y. C., Yao, J., Adamczyk, J., & Luttrell, R. (2017). Feeding toxicity and impact of imidacloprid formulation and mixtures with six representative pesticides at residue concentrations on honey bee physiology (Apis mellifera). PLoS ONE, 12, e0178421. https://doi.org/10.1371/journal.pone.0178421

Auteurs

Marco Paoli (M)

Neuroscience Paris-Seine, Institut de Biologie Paris-Seine, CNRS, INSERM, Sorbonne University, Paris, France.

Martin Giurfa (M)

Neuroscience Paris-Seine, Institut de Biologie Paris-Seine, CNRS, INSERM, Sorbonne University, Paris, France.
Institut Universitaire de France, Paris, France.

Classifications MeSH