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Effect of Sub-lethal Doses of Imidacloprid on Learning and Memory Formation of Indigenous Arabian Bee (Apis mellifera jemenitica Ruttner) Adult Foragers

  • J IqbalEmail author
  • A S Alqarni
  • H S A Raweh
Ecology, Behavior and Bionomics

Abstract

The indigenous bee race Apis mellifera jemenitica Ruttner of Saudi Arabia can learn and retain memories established by the classical conditioning of proboscis extension response (PER). The insecticide imidacloprid has shown a drastic effect on the olfactory behavior of A. m. jemenitica in the harsh arid climatic conditions of central Saudi Arabia. The oral feeding of single imidacloprid sub-lethal doses (1.0 ng, 0.5 ng, or 0.1 ng) under laboratory conditions significantly impaired associative learning during the 2nd and 3rd conditioning trials compared to control bees (0 ng). The memory tests also revealed significant impairment in memory formation at 1 h, 2 h, and 24 h after conditioning compared to control bees. Even the lowest dose (0.1 ng/bee) can significantly impair the bees’ ability to learn and memorize. This impairment effect was dose dependent and increased with increasing doses. The higher dose (1.0 ng) completely impaired the learning but still showed a little memory and reflected the potential recovery of bees from insecticide-induced impairment with the passage of time. To our knowledge, this is the first study in A. m. jemenitica that demonstrated the drastic effect of neonicotinoids on associative learning in indigenous bees. This study further expresses the possible severity of insecticidal exposure to bees in actual field conditions and its effect on the neural functions used in important behavior involved in the foraging of bees.

Keywords

Insecticide neonicotinoid associative learning honey bee Apis mellifera jemenitica 

Notes

Acknowledgement

This work was supported by the Deanship of Scientific Research, King Saud University, Riyadh, Saudi Arabia, project number RGP-189.

Author Contributions

JI designed, executed, analyzed the data and wrote the initial manuscript, ASA reviewed the results, figures, and the final manuscript, and HSAR helped in the execution and data collection of the experiments.

References

  1. Abou-Shaara HF (2014) The foraging behaviour of honey bees, Apis mellifera: a review. Vet Med-Czech 59(1):1–10.  https://doi.org/10.17221/7240-VETMED CrossRefGoogle Scholar
  2. Abou-Shaara HF, Owayss AA, Ibrahim YY, Basuny NK (2017) A review of impacts of temperature and relative humidity on various activities of honey bees. Insect Soc 64(4):455–463.  https://doi.org/10.1007/s00040-017-0573-8 CrossRefGoogle Scholar
  3. Aktar MW, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2(1):1–12.  https://doi.org/10.2478/v10102-009-0001-7 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alattal Y, Al Ghamdi A, Al Sharhi M, Fuchs S (2014) Morphometric characterisation of the native honeybee, Apis mellifera Linnaeus, 1758, of Saudi Arabia. Zool Middle East 60(3):226–235.  https://doi.org/10.1080/09397140.2014.944431 CrossRefGoogle Scholar
  5. Ali MAM (2011) Comparative study for evaluating two honey bee races, Apis mellifera jementica (indigenous race) and Apis mellifera carnica (carniolan race) in brood production, population development and foraging activity under the environmental conditions of the central region of the Kingdom of Saudi Arabia. Ann Agric Sci 56(2):127–134.  https://doi.org/10.1016/j.aoas.2011.07.006 CrossRefGoogle Scholar
  6. Ali H, Alqarni AS, Owayss AA, Hassan AM, Smith BH (2017) Osmotic concentration in three races of honey bee, Apis mellifera L. under environmental conditions of arid zone. Saudi J Biol Sci 24(5):1081–1085.  https://doi.org/10.1016/j.sjbs.2016.12.006 CrossRefPubMedGoogle Scholar
  7. Aljedani DM (2017) Effects of abamectin and deltamethrin to the foragers honeybee workers of Apis mellifera jemenatica (Hymenoptera: Apidae) under laboratory conditions. Saudi J Biol Sci 24(5):1007–1015.  https://doi.org/10.1016/j.sjbs.2016.12.007 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Aljedani DM, Almehmadi RM (2016) Effects of some insecticides on longevity of the foragers honey bee worker of local honey bee race Apis mellifera jemenatica. Electronic Physician 8(1):1843–1849.  https://doi.org/10.19082/1843b CrossRefPubMedPubMedCentralGoogle Scholar
  9. Alqarni AS, Hannan MA, Owayss AA, Engel MS (2011) The indigenous honey bees of Saudi Arabia (Hymenoptera, Apidae, Apis mellifera jemenitica Ruttner): their natural history and role in beekeeping. Zookeys 134(134):83–98.  https://doi.org/10.3897/zookeys.134.1677 CrossRefGoogle Scholar
  10. Alqarni AS, Balhareth HM, Owayss AA (2014) Performance evaluation of indigenous and exotic honey bee (Apis mellifera L.) races in Assir region, southwestern Saudi Arabia. Saudi J Biol Sci 21(3):256–264.  https://doi.org/10.1016/j.sjbs.2013.10.007 CrossRefPubMedGoogle Scholar
  11. Blacquiere T, Smagghe G, van Gestel CA, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21(4):973–992.  https://doi.org/10.1007/s10646-012-0863-x CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bonmatin JM, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, Marzaro M, Mitchell EA, Noome DA, Simon-Delso N, Tapparo A (2015) Environmental fate and exposure; neonicotinoids and fipronil. Environ Sci Pollut Res Int 22(1):35–67.  https://doi.org/10.1007/s11356-014-3332-7 CrossRefPubMedGoogle Scholar
  13. Ciarlo TJ, Mullin CA, Frazier JL, Schmehl DR (2012) Learning impairment in honey bees caused by agricultural spray adjuvants. PLoS One 7(7):e40848.  https://doi.org/10.1371/journal.pone.0040848 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Codling G, Al Naggar Y, Giesy JP, Robertson AJ (2016) Concentrations of neonicotinoid insecticides in honey, pollen and honey bees (Apis mellifera L.) in central Saskatchewan, Canada. Chemosphere 144:2321–2328.  https://doi.org/10.1016/j.chemosphere.2015.10.135 CrossRefPubMedGoogle Scholar
  15. Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20(1):149–157.  https://doi.org/10.1007/s10646-010-0566-0 CrossRefPubMedGoogle Scholar
  16. Decourtye A, Lacassie E, Pham-Delegue MH (2003) Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59(3):269–278.  https://doi.org/10.1002/ps.631 CrossRefPubMedGoogle Scholar
  17. Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delegue MH (2004) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57(3):410–419.  https://doi.org/10.1016/j.ecoenv.2003.08.001 CrossRefPubMedGoogle Scholar
  18. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106.  https://doi.org/10.1146/annurev.ento.52.110405.091440 CrossRefGoogle Scholar
  19. Dively GP, Embrey MS, Kamel A, Hawthorne DJ, Pettis JS (2015) Assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLoS One 10(3):e0118748.  https://doi.org/10.1371/journal.pone.0118748 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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(3):e91364.  https://doi.org/10.1371/journal.pone.0091364 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Forfert N, Troxler A, Retschnig G, Gauthier L, Straub L, Moritz RFA, Neumann P, Williams GR (2017) Neonicotinoid pesticides can reduce honeybee colony genetic diversity. PLoS One 12(10):e0186109.  https://doi.org/10.1371/journal.pone.0186109 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Frost EH, Shutler D, Hillier NK (2013) Effects of fluvalinate on honey bee learning, memory, responsiveness to sucrose, and survival. J Exp Biol 216(15):2931–2938.  https://doi.org/10.1242/jeb.086538 CrossRefPubMedGoogle Scholar
  23. Gauthier M (2010) State of the art on insect nicotinic acetylcholine receptor function in learning and memory. In: Thany SH (ed) Insect nicotinic acetylcholine receptors. Springer, New York, pp 97–115.  https://doi.org/10.1007/978-1-4419-6445-8_9 CrossRefGoogle Scholar
  24. Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C, Büchler R, Berg S, Ritter W, Mühlen W, Gisder S, Meixner M, Liebig G, Rosenkranz P (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41(3):332–352.  https://doi.org/10.1051/apido/2010014 CrossRefGoogle Scholar
  25. Giurfa M, Sandoz JC (2012) Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learn Memory 19(2):54–66.  https://doi.org/10.1101/lm.024711.111 CrossRefGoogle Scholar
  26. Gonalons C, Farina WM (2015) Effects of sublethal doses of imidacloprid on young adult honeybee behaviour. PLoS One 10(10):e0140814.  https://doi.org/10.1371/journal.pone.0140814 CrossRefGoogle Scholar
  27. Goulson D (2013) Review: an overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50(4):977–987.  https://doi.org/10.1111/1365-2664.12111 CrossRefGoogle Scholar
  28. Iqbal J, Mueller U (2007) Virus infection causes specific learning deficits in honeybee foragers. Proc R Soc Lond B Biol Sci 274(1617):1517–1521.  https://doi.org/10.1098/rspb.2007.0022 CrossRefGoogle Scholar
  29. Iqbal J, Ali H, Owayss AA, Raweh HSA, Engel MS, Alqarni AS, Smith BH (2018) Olfactory associative behavioral differences in three honey bee Apis mellifera L. races under the arid zone ecosystem of central Saudi Arabia. Saudi J Biol Sci.  https://doi.org/10.1016/j.sjbs.2018.08.002
  30. Jacques A, Laurent M, Ribiere-Chabert M, Saussac M, Bougeard S, Budge GE, Hendrikx P, Chauzat MP, De Graaf D, Meroc E, Nguyen BK, Roelandt S, Roels S, Van der Stede Y, Tonnersen T, Kryger P, Jaarma K, Kuus M, Raie A, Heinikainen S, Pelkonen S, Vahanikkila N, Andrieux C, Ballis A, Barrieu G, Bendali F, Brugoux C, Franco S, Fuentes AM, Joel A, Layec Y, Lopez J, Lozach A, Malherbe DL, Mariau V, Meziani F, Monod D, Mutel S, Oesterle E, Orlowski M, Petit M, Pillu P, Poret F, Viry A, Berg S, Buchler R, de Craigher D, Genersch E, Kaatz HH, Meixner MD, von der Ohe W, Otten C, Rosenkranz P, Schaefer MO, Schroeder A, Agianiotaki E, Arfara S, Boutsini S, Giannoulopoulou M, Hondrou V, Karipidou S, Katsaros D, Katzagiannakis A, Kiriakopoulos A, Oureilidis K, Panteli A, Pantoleon F, Papagianni Z, Papalexiou E, Perdikaris S, Prapas A, Siana P, Skandalakis I, Stougiou D, Tomazinakis I, Tsali E, Tseliou E, Tsiplakidis A, Tsompanellis E, Vamvakas G, Varvarouta V, Vourvidis D, Dan A, Daroczi G, Lang M, Papp M, Paulus PD, Pupp E, Szalo M, Toth A, Zseli S, Bressan G, Cerrone A, Formato G, Granato A, Lavazza A, Macellari P, Marcello P, Ghittino C, Maroni PA, Possidente R, Mutinelli F, Nassuato C, Pintore A, Ricchiuti L, Ruocco L, Salvaggio A, Troiano P, Voltini B, Avsejenko J, Ciekure E, Deksne G, Eglite I, Granta R, Olsevski E, Rodze I, Stinka M, Sirutkaityte R, Siriukaitis S, Bober A, Jazdzewski K, Pohorecka K, Skubida M, Zdanska D, Amador MRR, Freitas S, Quintans S, Santos PT, Brezinova N, Brtkova A, Cuvalova Z, Filipova M, Jurovcikova J, Kantikova M, Kubicova Z, Papiernikova E, Sulejova L, Toporcak J, Ares CCM, Ariza J, Berna SN, Cabeza NA, Casasempere CJ, Cid GC, Corzan RJM, De Abajo DMA, Diaz RR, Esteban RA, Fernandez SP, Garcia PA, Gonzalez BC, Minguez GO, Onate ML, Oteiza OP, Perez CI, Plaza PM, Puy P, Riol GR, Romero GLJ, Soldevilla YJF, Barrasus MSI, Soriano GM, Vigo LV, Villarta RJL, Fabricius-Kristiansen L, Forsgren E, Brown M, Budge G, Grant R, Marris G, Powell M, Wattam A, Whiting I, Cauquil L, Riviere MP, Garin E, Consortium E (2017) A pan-European epidemiological study reveals honey bee colony survival depends on beekeeper education and disease control. PLoS One 12(3):17.  https://doi.org/10.1371/journal.pone.0172591 CrossRefGoogle Scholar
  31. Jeschke P, Nauen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59(7):2897–2908.  https://doi.org/10.1021/jf101303g CrossRefPubMedGoogle Scholar
  32. Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity - USA. Apidologie 41(3):312–331.  https://doi.org/10.1051/apido/2010018 CrossRefGoogle Scholar
  33. Kiljanek T, Niewiadowska A, Posyniak A (2016) Pesticide poisoning of honeybees: a review of symptoms, incident classification, and causes of poisoning. J Apic Sci 60(2):5–24.  https://doi.org/10.1515/jas-2016-0024 CrossRefGoogle Scholar
  34. Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One 7(1):e29268.  https://doi.org/10.1371/journal.pone.0029268 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Laurino D, Manino A, Patetta A, Porporato M (2013) Toxicity of neonicotinoid insecticides on different honey bee genotypes. B Insectol 66(1):119–126Google Scholar
  36. Lundin O, Rundlof M, Smith HG, 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(8):e0136928.  https://doi.org/10.1371/journal.pone.0136928 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Manjon C, Troczka BJ, Zaworra M, Beadle K, Randall E, Hertlein G, Singh KS, Zimmer CT, Homem RA, Lueke B, Reid R, Kor L, Kohler M, Benting J, Williamson MS, Davies TGE, Field LM, Bass C, Nauen R (2018) Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Curr Biol 28(7):1137–1143.e1135.  https://doi.org/10.1016/j.cub.2018.02.045 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Menzel R, Müller U (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19:379–404.  https://doi.org/10.1146/annurev.ne.19.030196.002115 CrossRefPubMedGoogle Scholar
  39. Merschbaecher K, Haettig J, Mueller U (2012) Acetylation-mediated suppression of transcription-independent memory: bidirectional modulation of memory by acetylation. PLoS One 7(9):e45131.  https://doi.org/10.1371/journal.pone.0045131 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Michely J, Kraft S, Muller U (2017) miR-12 and miR-124 contribute to defined early phases of long-lasting and transient memory. Sci Rep 7:7910.  https://doi.org/10.1038/s41598-017-08486-w CrossRefPubMedPubMedCentralGoogle Scholar
  41. Müller U (2002) Learning in honeybees: from molecules to behaviour. Zoology (Jena, Germany) 105(4):313–320.  https://doi.org/10.1078/0944-2006-00075 CrossRefGoogle Scholar
  42. Müller U (2013) Memory phases and signaling cascades in honeybees. In: Menzel R, Benjamin PR (eds) Handbook of behavioral neuroscience, vol 22. Elsevier press, Philadelphia, pp 433–441.  https://doi.org/10.1016/B978-0-12-415823-8.00031-9 CrossRefGoogle Scholar
  43. 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 Manag Sci 57(7):577–586.  https://doi.org/10.1002/ps.331 CrossRefPubMedGoogle Scholar
  44. Ndakidemi B, Mtei K, Ndakidemi PA (2016) Impacts of synthetic and botanical pesticides on beneficial insects. Agric Sci 7(6):364–372Google Scholar
  45. Nicolopoulou-Stamati P, Maipas S, Kotampasi C, Stamatis P, Hens L (2016) Chemical pesticides and human health: the urgent need for a new concept in agriculture. Front Public Health 4:148.  https://doi.org/10.3389/fpubh.2016.00148 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Odemer R, Nilles L, Linder N, Rosenkranz P (2018) Sublethal effects of clothianidin and Nosema spp. on the longevity and foraging activity of free flying honey bees. Ecotoxicology 27(5):527–538.  https://doi.org/10.1007/s10646-018-1925-5 CrossRefPubMedGoogle Scholar
  47. Peng YC, Yang EC (2016) Sublethal dosage of imidacloprid reduces the microglomerular density of honey bee mushroom bodies. Sci Rep 6:192–198.  https://doi.org/10.1038/srep19298 CrossRefGoogle Scholar
  48. Pisa L, Goulson D, Yang E-C, Gibbons D, Sánchez-Bayo F, Mitchell E, Aebi A, van der Sluijs J, MacQuarrie CJK, Giorio C, Long EY, McField M, Bijleveld van Lexmond M, Bonmatin J-M (2017) An update of the worldwide integrated assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems. Environ Sci Pollut Res:1–49.  https://doi.org/10.1007/s11356-017-0341-3
  49. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25(6):345–353.  https://doi.org/10.1016/j.tree.2010.01.007 CrossRefPubMedGoogle Scholar
  50. Retschnig G, Williams GR, Odemer R, Boltin J, Di Poto C, Mehmann MM, Retschnig P, Winiger P, Rosenkranz P, Neumann P (2015) Effects, but no interactions, of ubiquitous pesticide and parasite stressors on honey bee (Apis mellifera) lifespan and behaviour in a colony environment. Environ Microbiol 17(11):4322–4331.  https://doi.org/10.1111/1462-2920.12825 CrossRefPubMedGoogle Scholar
  51. Rolke D, Fuchs S, Grunewald B, Gao Z, Blenau W (2016) Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in northern Germany: effects on honey bees (Apis mellifera). Ecotoxicology 25(9):1648–1665.  https://doi.org/10.1007/s10646-016-1725-8 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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(1):71–83CrossRefGoogle Scholar
  53. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119.  https://doi.org/10.1016/j.jip.2009.07.016 CrossRefPubMedGoogle Scholar
  54. Ruttner F (1976) Les races d’abeilles de l’Afrique. Paper presented at the XXV Congrés International d’Apiculture, Grenoble, FranceGoogle Scholar
  55. Sanchez-Bayo F, Goka K (2014) Pesticide residues and bees - a risk assessment. PLoS One 9(4):e94482.  https://doi.org/10.1371/journal.pone.0094482 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sanchez-Bayo F, Goka K (2016) Impacts of pesticides on honey bees. In: Chambo DE (eds) Beekeeping and bee conservation - advances in research. InTech Publishers, pp 77–97.  https://doi.org/10.5772/62487 Google Scholar
  57. Schmuck R, Schoning R, Stork A, Schramel O (2001) Risk posed to honeybees (Apis mellifera L. Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 57(3):225–238.  https://doi.org/10.1002/ps.270 CrossRefPubMedGoogle Scholar
  58. Siede R, Meixner MD, Almanza MT, Schoning R, Maus C, Buchler R (2018) A long-term field study on the effects of dietary exposure of clothianidin to varroosis-weakened honey bee colonies. Ecotoxicology 27(7):772–783.  https://doi.org/10.1007/s10646-018-1937-1 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Smith BH, Burden CM (2014) A proboscis extension response protocol for investigating behavioral plasticity in insects: application to basic, biomedical, and agricultural research. Jove-J Vis Exp 91:e51057.  https://doi.org/10.3791/51057 CrossRefGoogle Scholar
  60. Sponsler DB, Johnson RM (2017) Mechanistic modeling of pesticide exposure: the missing keystone of honey bee toxicology. Environ Toxicol Chem 36(4):871–881.  https://doi.org/10.1002/etc.3661 CrossRefPubMedGoogle Scholar
  61. Straub L, Williams GR, Pettis J, Fries I, Neumann P (2015) Superorganism resilience: eusociality and susceptibility of ecosystem service providing insects to stressors. Curr Opin Insect Sci 12:109–112.  https://doi.org/10.1016/j.cois.2015.10.010 CrossRefGoogle Scholar
  62. Tan K, Chen WW, Dong SH, Liu XW, Wang YC, Nieh JC (2014) Imidacloprid alters foraging and decreases bee avoidance of predators. PLoS One 9(7):e102725.  https://doi.org/10.1371/journal.pone.0102725 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Tan K, Chen WW, Dong SH, Liu XW, Wang YC, Nieh JC (2015) A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Sci Rep 5:10989.  https://doi.org/10.1038/srep10989 CrossRefPubMedPubMedCentralGoogle Scholar
  64. van der Sluijs JP, Vaage NS (2016) Pollinators and global food security: the need for holistic global stewardship. Food Ethics 1(1):75–91.  https://doi.org/10.1007/s41055-016-0003-z CrossRefGoogle Scholar
  65. Wang ZW, Tan K (2014) Comparative analysis of olfactory learning of Apis cerana and Apis mellifera. Apidologie 45(1):45–52.  https://doi.org/10.1007/s13592-013-0228-3 CrossRefGoogle Scholar
  66. Williamson SM, Wright GA (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 216(10):1799–1807CrossRefGoogle Scholar
  67. Wood TJ, Goulson D (2017) The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ Sci Pollut Res Int 24(21):17285–17325.  https://doi.org/10.1007/s11356-017-9240-x CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yang EC, Chuang YC, Chen YL, Chang LH (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 101(6):1743–1748.  https://doi.org/10.1603/0022-0493-101.6.1743 CrossRefPubMedGoogle Scholar
  69. Zhou T, Song H-L, Wang Q, Dai P-L, Wu Y-Y, Sun J-H (2013) Effects of imidacloprid on the distribution of nicotine acetylcholine receptors in the brain of adult honeybee (Apis mellifera ligustica). Acta Entomol Sin 56(11):1258–1266Google Scholar

Copyright information

© Sociedade Entomológica do Brasil 2018

Authors and Affiliations

  1. 1.Melittology Research Lab, Dept of Plant Protection, College of Food and Agriculture SciencesKing Saud UnivRiyadhSaudi Arabia
  2. 2.Dept of EntomologyMNS Univ of AgricultureMultanPakistan

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