Acetylcholine and Its Receptors in Honeybees: Involvement in Development and Impairments by Neonicotinoids

Acetylcholine (ACh) is the major excitatory neurotransmitter in the insect central nervous system (CNS). However, besides the neuronal expression of ACh receptors (AChR), the existence of non-neuronal AChR in honeybees is plausible. The cholinergic system is a popular target of insecticides because...

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Published inInsects (Basel, Switzerland) Vol. 10; no. 12; p. 420
Main Authors Grünewald, Bernd, Siefert, Paul
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 22.11.2019
MDPI
Subjects
Acetylcholine
Acetylcholine receptors (nicotinic)
Bees
Behavior
Central nervous system
Cholinergic transmission
Cholinergics
Developmental stages
Food
Gene expression
Hypopharyngeal gland
Insecticides
Insects
Larval development
Livestock
Nervous system
Neurons
Neurotransmitters
Permeability
Pesticides
Pharmacology
Plant protection
Receptors
Review
Royal jelly
Signal transduction
Vertebrates
Apis mellifera
larvae
insecticides
nicotinic acetylcholine receptors
brood
royal jelly
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Abstract Acetylcholine (ACh) is the major excitatory neurotransmitter in the insect central nervous system (CNS). However, besides the neuronal expression of ACh receptors (AChR), the existence of non-neuronal AChR in honeybees is plausible. The cholinergic system is a popular target of insecticides because the pharmacology of insect nicotinic acetylcholine receptors (nAChRs) differs substantially from their vertebrate counterparts. Neonicotinoids are agonists of the nAChR and are largely used in crop protection. In contrast to their relatively high safety for humans and livestock, neonicotinoids pose a threat to pollinating insects such as bees. In addition to its effects on behavior, it becomes increasingly evident that neonicotinoids affect developmental processes in bees that appear to be independent of neuronal AChRs. Brood food (royal jelly, worker jelly, or drone jelly) produced in the hypopharyngeal glands of nurse bees contains millimolar concentrations of ACh, which is required for proper larval development. Neonicotinoids reduce the secreted ACh-content in brood food, reduce hypopharyngeal gland size, and lead to developmental impairments within the colony. We assume that potential hazards of neonicotinoids on pollinating bees occur neuronally causing behavioral impairments on adult individuals, and non-neuronally causing developmental disturbances as well as destroying gland functioning.
AbstractList Acetylcholine (ACh) is the major excitatory neurotransmitter in the insect central nervous system (CNS). However, besides the neuronal expression of ACh receptors (AChR), the existence of non-neuronal AChR in honeybees is plausible. The cholinergic system is a popular target of insecticides because the pharmacology of insect nicotinic acetylcholine receptors (nAChRs) differs substantially from their vertebrate counterparts. Neonicotinoids are agonists of the nAChR and are largely used in crop protection. In contrast to their relatively high safety for humans and livestock, neonicotinoids pose a threat to pollinating insects such as bees. In addition to its effects on behavior, it becomes increasingly evident that neonicotinoids affect developmental processes in bees that appear to be independent of neuronal AChRs. Brood food (royal jelly, worker jelly, or drone jelly) produced in the hypopharyngeal glands of nurse bees contains millimolar concentrations of ACh, which is required for proper larval development. Neonicotinoids reduce the secreted ACh-content in brood food, reduce hypopharyngeal gland size, and lead to developmental impairments within the colony. We assume that potential hazards of neonicotinoids on pollinating bees occur neuronally causing behavioral impairments on adult individuals, and non-neuronally causing developmental disturbances as well as destroying gland functioning.Acetylcholine (ACh) is the major excitatory neurotransmitter in the insect central nervous system (CNS). However, besides the neuronal expression of ACh receptors (AChR), the existence of non-neuronal AChR in honeybees is plausible. The cholinergic system is a popular target of insecticides because the pharmacology of insect nicotinic acetylcholine receptors (nAChRs) differs substantially from their vertebrate counterparts. Neonicotinoids are agonists of the nAChR and are largely used in crop protection. In contrast to their relatively high safety for humans and livestock, neonicotinoids pose a threat to pollinating insects such as bees. In addition to its effects on behavior, it becomes increasingly evident that neonicotinoids affect developmental processes in bees that appear to be independent of neuronal AChRs. Brood food (royal jelly, worker jelly, or drone jelly) produced in the hypopharyngeal glands of nurse bees contains millimolar concentrations of ACh, which is required for proper larval development. Neonicotinoids reduce the secreted ACh-content in brood food, reduce hypopharyngeal gland size, and lead to developmental impairments within the colony. We assume that potential hazards of neonicotinoids on pollinating bees occur neuronally causing behavioral impairments on adult individuals, and non-neuronally causing developmental disturbances as well as destroying gland functioning.
Acetylcholine (ACh) is the major excitatory neurotransmitter in the insect central nervous system (CNS). However, besides the neuronal expression of ACh receptors (AChR), the existence of non-neuronal AChR in honeybees is plausible. The cholinergic system is a popular target of insecticides because the pharmacology of insect nicotinic acetylcholine receptors (nAChRs) differs substantially from their vertebrate counterparts. Neonicotinoids are agonists of the nAChR and are largely used in crop protection. In contrast to their relatively high safety for humans and livestock, neonicotinoids pose a threat to pollinating insects such as bees. In addition to its effects on behavior, it becomes increasingly evident that neonicotinoids affect developmental processes in bees that appear to be independent of neuronal AChRs. Brood food (royal jelly, worker jelly, or drone jelly) produced in the hypopharyngeal glands of nurse bees contains millimolar concentrations of ACh, which is required for proper larval development. Neonicotinoids reduce the secreted ACh-content in brood food, reduce hypopharyngeal gland size, and lead to developmental impairments within the colony. We assume that potential hazards of neonicotinoids on pollinating bees occur neuronally causing behavioral impairments on adult individuals, and non-neuronally causing developmental disturbances as well as destroying gland functioning.
Author Siefert, Paul
Grünewald, Bernd
AuthorAffiliation Institut für Bienenkunde, Polytechnische Gesellschaft, FB Biowissenschaften, Goethe-Universität Frankfurt am Main, Karl-von-Frisch-Weg 2, D-61440 Oberursel, Germany; siefert@bio.uni-frankfurt.de
AuthorAffiliation_xml – name: Institut für Bienenkunde, Polytechnische Gesellschaft, FB Biowissenschaften, Goethe-Universität Frankfurt am Main, Karl-von-Frisch-Weg 2, D-61440 Oberursel, Germany; siefert@bio.uni-frankfurt.de
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  givenname: Bernd
  surname: Grünewald
  fullname: Grünewald, Bernd
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  fullname: Siefert, Paul
  organization: Institut für Bienenkunde, Polytechnische Gesellschaft, FB Biowissenschaften, Goethe-Universität Frankfurt am Main, Karl-von-Frisch-Weg 2, D-61440 Oberursel, Germany
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Cites_doi 10.1007/BF00258746
10.1051/apido:19880103
10.1051/apido/2010043
10.1007/s10158-007-0062-2
10.1002/ps.1631
10.1038/s41598-017-04734-1
10.1002/ps.1446
10.1051/apido:2004068
10.1080/00218839.2016.1211394
10.1126/science.1215039
10.1007/s00359-004-0530-7
10.1016/j.ibmb.2017.01.011
10.1016/j.jinsphys.2012.03.015
10.1254/jjp.85.2
10.1146/annurev.en.14.010169.002131
10.1111/jnc.13953
10.1007/s10646-012-0863-x
10.11606/issn.2526-3382.bffclzoologia.1965.120680
10.1152/jn.1994.71.2.808
10.1515/bchm2.1955.301.1-2.78
10.1007/s00360-015-0934-4
10.1016/j.pestbp.2004.03.002
10.1007/978-1-4419-6445-8
10.3390/insects10010018
10.1016/S0304-3940(01)02400-4
10.1007/s13592-017-0533-3
10.1038/188854a0
10.1038/bjp.2008.185
10.1146/annurev.ento.48.091801.112731
10.1038/srep00288
10.1038/srep11779
10.1002/1526-4998(200009)56:9<784::AID-PS208>3.0.CO;2-T
10.1007/s11356-017-9240-x
10.1007/978-1-4419-6445-8_5
10.1002/ps.5124
10.1126/science.aaa1190
10.1371/journal.pone.0156886
10.1007/s00359-005-0007-3
10.1002/ps.331
10.1007/978-3-642-57079-7
10.1016/j.jinsphys.2016.01.001
10.1098/rspb.2014.0558
10.1002/cne.902860105
10.1146/annurev-ento-020117-043042
10.1007/s13592-013-0199-4
10.1016/j.gene.2004.09.010
10.1007/s13592-015-0424-4
10.1046/j.1365-2583.2003.00409.x
10.1038/s41586-018-0430-6
10.1016/j.ecoenv.2019.05.007
10.3390/insects10100344
10.1098/rspb.2015.1821
10.1007/BF00640341
10.1007/978-1-4419-6445-8_8
10.1007/BF00628720
10.1007/BF00301617
10.1007/s13592-016-0435-9
10.1371/journal.pone.0030023
10.1111/j.1469-7793.1999.759ad.x
10.1021/acs.est.6b02658
10.1603/0022-0493(2007)100[1188:CILOJH]2.0.CO;2
10.1007/s13592-012-0135-z
10.1051/apido/2009051
10.1371/journal.pone.0048838
10.1002/jcp.1030350103
10.1007/978-94-007-2099-2
10.1007/s13592-017-0506-6
10.1038/srep38110
10.1007/978-1-4419-6445-8_9
10.1002/wsbm.73
10.1016/j.nlm.2006.02.003
10.1111/j.2041-210X.2011.00099.x
10.1177/0192623319877154
10.1146/annurev.pharmtox.45.120403.095930
10.1038/nature14420
10.1111/afe.12041
10.1038/srep05566
10.1038/srep29608
10.1111/j.1365-2583.2006.00672.x
10.1007/s00018-013-1334-0
10.1101/105700
10.1021/acs.est.6b04791
10.1371/journal.pone.0091364
10.1371/journal.pone.0014720
10.1371/journal.pone.0171529
10.1016/j.envpol.2018.09.117
10.1002/arch.10022
10.1002/anie.201302550
10.1016/j.jinsphys.2014.10.002
10.1016/B978-0-12-415823-8.00035-6
10.1016/j.ecoenv.2017.08.047
10.1016/0006-8993(90)91805-Q
10.1371/journal.pone.0068191
10.1603/0022-0493(2008)101[784:LASEOI]2.0.CO;2
10.1016/0306-4492(81)90121-0
10.1016/S0166-4328(96)89081-4
10.1111/imb.12229
10.1371/journal.pone.0049472
10.1038/s41598-017-10489-6
10.1021/acs.est.6b00678
10.1139/z59-081
10.1101/gr.4549206
10.1007/s10646-016-1725-8
10.1038/ncomms2648
10.1152/jn.00126.2011
10.1007/978-1-4419-6445-8_3
10.1016/S0304-3940(99)00694-1
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Issue 12
Keywords Apis mellifera
larvae
insecticides
nicotinic acetylcholine receptors
brood
royal jelly
Language English
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References ref_14
ref_13
Ament (ref_92) 2010; 2
Heylen (ref_97) 2011; 42
ref_99
Rondeau (ref_41) 2015; 4
Sandrock (ref_42) 2014; 16
Baines (ref_104) 2017; 7
ref_19
Thany (ref_24) 2003; 12
Siviter (ref_47) 2018; 561
Bischoff (ref_88) 2018; 49
Bicker (ref_64) 1994; 71
(ref_17) 2013; 22
Jeschke (ref_68) 2013; 52
Godfray (ref_58) 2014; 281
Rockstein (ref_91) 1950; 35
Woodcock (ref_43) 2017; 356
Henry (ref_49) 2012; 336
Mogren (ref_114) 2016; 6
ref_27
Claudianos (ref_113) 2006; 15
Christen (ref_109) 2016; 50
Crailsheim (ref_95) 1992; 162
Kou (ref_108) 2002; 49
Godfray (ref_59) 2015; 282
Palmer (ref_34) 2013; 4
ref_76
Andersson (ref_44) 2015; 521
Sastry (ref_1) 1978; 30
Barbara (ref_62) 2008; 8
Lozano (ref_69) 1996; 81
Jones (ref_26) 2010; 683
Gregorc (ref_111) 2012; 58
ref_83
Henschler (ref_81) 1960; 47
Gauthier (ref_33) 2002; 321
Rand (ref_116) 2015; 5
Rolke (ref_45) 2016; 25
Wood (ref_60) 2017; 24
Thany (ref_18) 2010; 683
Russell (ref_6) 2004; 79
ref_86
Kim (ref_8) 2017; 7
Kreissl (ref_20) 1989; 286
Barbara (ref_22) 2005; 191
Deseyn (ref_93) 2005; 36
Oertner (ref_16) 1999; 274
Aupinel (ref_36) 2007; 63
Thany (ref_28) 2010; 683
Havstad (ref_48) 2019; 69
Tison (ref_54) 2019; 180
Cook (ref_105) 2019; 10
Casida (ref_29) 2018; 63
Nauen (ref_32) 2001; 57
Decourtye (ref_53) 2004; 78
Fischer (ref_50) 2014; 9
Lapied (ref_65) 1990; 533
Collin (ref_72) 2013; 70
Jeschke (ref_67) 2008; 64
Yu (ref_107) 2007; 100
Tan (ref_84) 2015; 5
ref_56
ref_55
Human (ref_117) 2017; 82
Teixeira (ref_39) 2016; 47
Ellis (ref_46) 2017; 51
Abbott (ref_87) 2008; 101
Grillone (ref_35) 2017; 48
Dai (ref_40) 2019; 75
Hatjina (ref_96) 2013; 44
(ref_80) 1966; 8
Decourtye (ref_85) 2010; 683
(ref_21) 2004; 190
Shuel (ref_79) 1959; 37
Henschler (ref_74) 1954; 41
Dupuis (ref_23) 2011; 106
Gauthier (ref_70) 2006; 86
Malloy (ref_10) 2016; 186
Lu (ref_9) 2012; 2
Wessler (ref_3) 2017; 142
Welsh (ref_77) 1965; 25
Wittmann (ref_89) 1982; 13
Renzi (ref_101) 2016; 47
Goldschmidt (ref_75) 1955; 301
Valente (ref_78) 1981; 69
Tison (ref_51) 2016; 50
Schmehl (ref_112) 2014; 71
Colhoun (ref_82) 1960; 188
Smallman (ref_5) 1969; 14
Tasei (ref_38) 2000; 56
Goldberg (ref_15) 1999; 514
ref_31
ref_110
Tomizawa (ref_30) 2003; 48
Andrione (ref_71) 2016; 6
Blacquiere (ref_57) 2012; 21
Christen (ref_103) 2018; 243
Wessler (ref_2) 2009; 154
Wilde (ref_115) 2016; 55
Crailsheim (ref_94) 1991; 161
Hendriksma (ref_37) 2011; 2
Tomizawa (ref_66) 2005; 45
ref_106
Himmelreich (ref_63) 2012; 43
Jones (ref_61) 2006; 16
ref_100
Gregorc (ref_98) 2010; 41
ref_102
Davis (ref_90) 1988; 19
Xia (ref_73) 2016; 25
Brandt (ref_12) 2017; 7
Brandt (ref_11) 2016; 86
Thany (ref_25) 2005; 344
Alkassab (ref_52) 2018; 147
Wessler (ref_4) 2001; 85
ref_7
References_xml – volume: 161
  start-page: 55
  year: 1991
  ident: ref_94
  article-title: Interadult feeding of jelly in honeybee (Apis mellifera L.) colonies
  publication-title: J. Comp. Physiol. B
  doi: 10.1007/BF00258746
  contributor:
    fullname: Crailsheim
– volume: 19
  start-page: 37
  year: 1988
  ident: ref_90
  article-title: Distribution of 14 C-labelled carbofuran and dimethoate in royal jelly, queen larvae and nurse honeybees
  publication-title: Apidologie
  doi: 10.1051/apido:19880103
  contributor:
    fullname: Davis
– volume: 42
  start-page: 103
  year: 2011
  ident: ref_97
  article-title: The effects of four crop protection products on the morphology and ultrastructure of the hypopharyngeal gland of the European honeybee, Apis mellifera
  publication-title: Apidologie
  doi: 10.1051/apido/2010043
  contributor:
    fullname: Heylen
– volume: 8
  start-page: 19
  year: 2008
  ident: ref_62
  article-title: Study of nicotinic acetylcholine receptors on cultured antennal lobe neurones from adult honeybee brains
  publication-title: Invertebr. Neurosci.
  doi: 10.1007/s10158-007-0062-2
  contributor:
    fullname: Barbara
– volume: 64
  start-page: 1084
  year: 2008
  ident: ref_67
  article-title: Neonicotinoids-from zero to hero in insecticide chemistry
  publication-title: Pest Manag. Sci.
  doi: 10.1002/ps.1631
  contributor:
    fullname: Jeschke
– volume: 7
  start-page: 4673
  year: 2017
  ident: ref_12
  article-title: Immunosuppression in honeybee queens by the neonicotinoids thiacloprid and clothianidin
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-017-04734-1
  contributor:
    fullname: Brandt
– volume: 5
  start-page: 1
  year: 2015
  ident: ref_84
  article-title: A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults
  publication-title: Sci. Rep.
  contributor:
    fullname: Tan
– ident: ref_100
– volume: 63
  start-page: 1090
  year: 2007
  ident: ref_36
  article-title: Toxicity of dimethoate and fenoxycarb to honey bee brood (Apis mellifera), using a newin vitro standardized feeding method
  publication-title: Pest Manag. Sci.
  doi: 10.1002/ps.1446
  contributor:
    fullname: Aupinel
– volume: 36
  start-page: 49
  year: 2005
  ident: ref_93
  article-title: Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera workers (Hymenoptera, Apidae)
  publication-title: Apidologie
  doi: 10.1051/apido:2004068
  contributor:
    fullname: Deseyn
– volume: 55
  start-page: 212
  year: 2016
  ident: ref_115
  article-title: The influence of sublethal doses of imidacloprid on protein content and proteolytic activity in honey bees (Apis mellifera L.)
  publication-title: J. Apic. Res.
  doi: 10.1080/00218839.2016.1211394
  contributor:
    fullname: Wilde
– volume: 336
  start-page: 348
  year: 2012
  ident: ref_49
  article-title: A common pesticide decreases foraging success and survival in honey bees
  publication-title: Science
  doi: 10.1126/science.1215039
  contributor:
    fullname: Henry
– volume: 190
  start-page: 807
  year: 2004
  ident: ref_21
  article-title: Pharmacology of the neuronal nicotinic acetylcholine receptor of cultured Kenyon cells of the honeybee, Apis mellifera
  publication-title: J. Comp. Physiol. A
  doi: 10.1007/s00359-004-0530-7
– volume: 82
  start-page: 41
  year: 2017
  ident: ref_117
  article-title: Proteomic and metabolomic analysis reveals rapid and extensive nicotine detoxification ability in honey bee larvae
  publication-title: Insect Biochem. Mol. Biol.
  doi: 10.1016/j.ibmb.2017.01.011
  contributor:
    fullname: Human
– volume: 58
  start-page: 1042
  year: 2012
  ident: ref_111
  article-title: Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor)
  publication-title: J. Insect Physiol.
  doi: 10.1016/j.jinsphys.2012.03.015
  contributor:
    fullname: Gregorc
– volume: 85
  start-page: 2
  year: 2001
  ident: ref_4
  article-title: The biological role of non-neuronal acetylcholine in plants and Humans
  publication-title: Jpn. J. Pharmacol.
  doi: 10.1254/jjp.85.2
  contributor:
    fullname: Wessler
– volume: 14
  start-page: 387
  year: 1969
  ident: ref_5
  article-title: The cholinergic system in insect development
  publication-title: Annu. Rev. Entomol.
  doi: 10.1146/annurev.en.14.010169.002131
  contributor:
    fullname: Smallman
– volume: 142
  start-page: 144
  year: 2017
  ident: ref_3
  article-title: Non-neuronal acetylcholine involved in reproduction in mammals and honeybees
  publication-title: J. Neurochem.
  doi: 10.1111/jnc.13953
  contributor:
    fullname: Wessler
– volume: 21
  start-page: 973
  year: 2012
  ident: ref_57
  article-title: Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment
  publication-title: Ecotoxicology
  doi: 10.1007/s10646-012-0863-x
  contributor:
    fullname: Blacquiere
– volume: 25
  start-page: 105
  year: 1965
  ident: ref_77
  article-title: Acetylcholine in the larval food, honey and stored pollen of a stingless bee, Melipona quadrifasciata
  publication-title: Bol. da Fac. Filos. Ciências e Let. Univ. São Paulo. Zool.
  doi: 10.11606/issn.2526-3382.bffclzoologia.1965.120680
  contributor:
    fullname: Welsh
– volume: 71
  start-page: 808
  year: 1994
  ident: ref_64
  article-title: Calcium imaging reveals nicotinic acetylcholine receptors on cultured mushroom body neurons
  publication-title: J. Neurophysiol.
  doi: 10.1152/jn.1994.71.2.808
  contributor:
    fullname: Bicker
– volume: 301
  start-page: 78
  year: 1955
  ident: ref_75
  article-title: Die Hydrolyse des cholinergischen Honigwirkstoffes und anderer Cholinester mittels Cholinesterasen und deren Hemmung im Honig
  publication-title: Hoppe Seyler´s Zeitschrift für Physiol. Chemie
  doi: 10.1515/bchm2.1955.301.1-2.78
  contributor:
    fullname: Goldschmidt
– volume: 186
  start-page: 45
  year: 2016
  ident: ref_10
  article-title: Pharmacological identification of cholinergic receptor subtypes on Drosophila melanogaster larval heart
  publication-title: J. Comp. Physiol. B Biochem. Syst. Environ. Physiol.
  doi: 10.1007/s00360-015-0934-4
  contributor:
    fullname: Malloy
– ident: ref_56
– volume: 79
  start-page: 84
  year: 2004
  ident: ref_6
  article-title: Two major classes of target site insensitivity mutations confer resistance to organophosphate and carbamate insecticides
  publication-title: Pestic. Biochem. Physiol.
  doi: 10.1016/j.pestbp.2004.03.002
  contributor:
    fullname: Russell
– ident: ref_14
  doi: 10.1007/978-1-4419-6445-8
– volume: 10
  start-page: 11
  year: 2019
  ident: ref_105
  article-title: Compound and dose-dependent effects of two neonicotinoid pesticides on honey bee (Apis mellifera) metabolic physiology
  publication-title: Insects
  doi: 10.3390/insects10010018
  contributor:
    fullname: Cook
– volume: 321
  start-page: 13
  year: 2002
  ident: ref_33
  article-title: The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells
  publication-title: Neurosci. Lett.
  doi: 10.1016/S0304-3940(01)02400-4
  contributor:
    fullname: Gauthier
– volume: 49
  start-page: 112
  year: 2018
  ident: ref_88
  article-title: From field to food—Will pesticide-contaminated pollen diet lead to a contamination of royal jelly?
  publication-title: Apidologie
  doi: 10.1007/s13592-017-0533-3
  contributor:
    fullname: Bischoff
– volume: 188
  start-page: 854
  year: 1960
  ident: ref_82
  article-title: Neurohormonal properties of royal jelly
  publication-title: Nature
  doi: 10.1038/188854a0
  contributor:
    fullname: Colhoun
– volume: 154
  start-page: 1558
  year: 2009
  ident: ref_2
  article-title: Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans
  publication-title: Br. J. Pharmacol.
  doi: 10.1038/bjp.2008.185
  contributor:
    fullname: Wessler
– volume: 48
  start-page: 339
  year: 2003
  ident: ref_30
  article-title: Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors
  publication-title: Annu. Rev. Entomol.
  doi: 10.1146/annurev.ento.48.091801.112731
  contributor:
    fullname: Tomizawa
– volume: 2
  start-page: 288
  year: 2012
  ident: ref_9
  article-title: Cholinergic and non-cholinergic functions of two acetylcholinesterase genes revealed by gene-silencing in Tribolium castaneum
  publication-title: Sci. Rep.
  doi: 10.1038/srep00288
  contributor:
    fullname: Lu
– volume: 5
  start-page: 11779
  year: 2015
  ident: ref_116
  article-title: Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine
  publication-title: Sci. Rep.
  doi: 10.1038/srep11779
  contributor:
    fullname: Rand
– volume: 56
  start-page: 784
  year: 2000
  ident: ref_38
  article-title: Sub-lethal effects of imidacloprid on bumblebees, Bombus terrestris (Hymenoptera: Apidae), during a laboratory feeding test
  publication-title: Pest Manag. Sci.
  doi: 10.1002/1526-4998(200009)56:9<784::AID-PS208>3.0.CO;2-T
  contributor:
    fullname: Tasei
– volume: 8
  start-page: 296
  year: 1966
  ident: ref_80
  article-title: Die Determination von Königin und Arbeiterin der Honigbiene
  publication-title: Z. Bienenforsch.
– volume: 24
  start-page: 17285
  year: 2017
  ident: ref_60
  article-title: The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013
  publication-title: Environ. Sci. Pollut. Res.
  doi: 10.1007/s11356-017-9240-x
  contributor:
    fullname: Wood
– ident: ref_106
– volume: 683
  start-page: 53
  year: 2010
  ident: ref_28
  article-title: Electrophysiological studies and pharmacological properties of insect native nicotinic acetylcholine receptors
  publication-title: Adv. Exp. Med. Biol.
  doi: 10.1007/978-1-4419-6445-8_5
  contributor:
    fullname: Thany
– volume: 75
  start-page: 29
  year: 2019
  ident: ref_40
  article-title: Chronic toxicity of clothianidin, imidacloprid, chlorpyrifos, and dimethoate to Apis mellifera L. larvae reared in vitro
  publication-title: Pest Manag. Sci.
  doi: 10.1002/ps.5124
  contributor:
    fullname: Dai
– volume: 356
  start-page: 1393
  year: 2017
  ident: ref_43
  article-title: Country-specific effects of neonicotinoid pesticides on honey bees and wild bees
  publication-title: Science
  doi: 10.1126/science.aaa1190
  contributor:
    fullname: Woodcock
– ident: ref_76
  doi: 10.1371/journal.pone.0156886
– volume: 191
  start-page: 823
  year: 2005
  ident: ref_22
  article-title: Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera
  publication-title: J. Comp. Physiol. A
  doi: 10.1007/s00359-005-0007-3
  contributor:
    fullname: Barbara
– volume: 57
  start-page: 577
  year: 2001
  ident: ref_32
  article-title: Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae)
  publication-title: Pest Manag. Sci.
  doi: 10.1002/ps.331
  contributor:
    fullname: Nauen
– ident: ref_27
  doi: 10.1007/978-3-642-57079-7
– volume: 86
  start-page: 40
  year: 2016
  ident: ref_11
  article-title: The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.)
  publication-title: J. Insect Physiol.
  doi: 10.1016/j.jinsphys.2016.01.001
  contributor:
    fullname: Brandt
– volume: 281
  start-page: 20140558
  year: 2014
  ident: ref_58
  article-title: A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators
  publication-title: Proc. R. Soc. B Biol. Sci.
  doi: 10.1098/rspb.2014.0558
  contributor:
    fullname: Godfray
– volume: 286
  start-page: 71
  year: 1989
  ident: ref_20
  article-title: Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee
  publication-title: J. Comp. Neurol.
  doi: 10.1002/cne.902860105
  contributor:
    fullname: Kreissl
– volume: 63
  start-page: 125
  year: 2018
  ident: ref_29
  article-title: Neonicotinoids and other insect nicotinic receptor competitive modulators: progress and prospects
  publication-title: Annu. Rev. Entomol.
  doi: 10.1146/annurev-ento-020117-043042
  contributor:
    fullname: Casida
– volume: 44
  start-page: 467
  year: 2013
  ident: ref_96
  article-title: Sublethal doses of imidacloprid decreased size of hypopharyngeal glands and respiratory rhythm of honeybees in vivo
  publication-title: Apidologie
  doi: 10.1007/s13592-013-0199-4
  contributor:
    fullname: Hatjina
– volume: 344
  start-page: 125
  year: 2005
  ident: ref_25
  article-title: Apisα2, Apisα7-1 and Apisα7-2: three new neuronal nicotinic acetylcholine receptor α-subunits in the honeybee brain
  publication-title: Gene
  doi: 10.1016/j.gene.2004.09.010
  contributor:
    fullname: Thany
– volume: 47
  start-page: 729
  year: 2016
  ident: ref_39
  article-title: Consumption of the neonicotinoid thiamethoxam during the larval stage affects the survival and development of the stingless bee, Scaptotrigona aff. depilis
  publication-title: Apidologie
  doi: 10.1007/s13592-015-0424-4
  contributor:
    fullname: Teixeira
– volume: 12
  start-page: 255
  year: 2003
  ident: ref_24
  article-title: Identification and localization of the nicotinic acetylcholine receptor alpha3 mRNA in the brain of the honeybee, Apis mellifera
  publication-title: Insect Mol. Biol.
  doi: 10.1046/j.1365-2583.2003.00409.x
  contributor:
    fullname: Thany
– volume: 561
  start-page: 109
  year: 2018
  ident: ref_47
  article-title: Sulfoxaflor exposure reduces bumblebee reproductive success
  publication-title: Nature
  doi: 10.1038/s41586-018-0430-6
  contributor:
    fullname: Siviter
– volume: 180
  start-page: 139
  year: 2019
  ident: ref_54
  article-title: The neonicotinoid clothianidin impairs memory processing in honey bees
  publication-title: Ecotoxicol. Environ. Saf.
  doi: 10.1016/j.ecoenv.2019.05.007
  contributor:
    fullname: Tison
– ident: ref_31
  doi: 10.3390/insects10100344
– volume: 282
  start-page: 20151821
  year: 2015
  ident: ref_59
  article-title: A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators
  publication-title: Proc. R. Soc. B Biol. Sci.
  doi: 10.1098/rspb.2015.1821
  contributor:
    fullname: Godfray
– volume: 41
  start-page: 142
  year: 1954
  ident: ref_74
  article-title: Hoher Acetylcholingehalt von Bienenfuttersäften
  publication-title: Naturwissenschaften
  doi: 10.1007/BF00640341
  contributor:
    fullname: Henschler
– volume: 683
  start-page: 85
  year: 2010
  ident: ref_85
  article-title: Ecotoxicity of neonicotinoid insecticides to bees
  publication-title: Adv. Exp. Med. Biol.
  doi: 10.1007/978-1-4419-6445-8_8
  contributor:
    fullname: Decourtye
– volume: 47
  start-page: 326
  year: 1960
  ident: ref_81
  article-title: Änderungen des Acetylcholingehaltes von Bienenfuttersäften in der Madenentwicklung
  publication-title: Naturwissenschaften
  doi: 10.1007/BF00628720
  contributor:
    fullname: Henschler
– volume: 162
  start-page: 681
  year: 1992
  ident: ref_95
  article-title: The flow of jelly within a honeybee colony
  publication-title: J. Comp. Physiol. B
  doi: 10.1007/BF00301617
  contributor:
    fullname: Crailsheim
– volume: 47
  start-page: 779
  year: 2016
  ident: ref_101
  article-title: Combined effect of pollen quality and thiamethoxam on hypopharyngeal gland development and protein content in Apis mellifera
  publication-title: Apidologie
  doi: 10.1007/s13592-016-0435-9
  contributor:
    fullname: Renzi
– volume: 7
  start-page: 1
  year: 2017
  ident: ref_8
  article-title: Expression of acetylcholinesterase 1 is associated with brood rearing status in the honey bee, Apis mellifera
  publication-title: Sci. Rep.
  contributor:
    fullname: Kim
– ident: ref_55
  doi: 10.1371/journal.pone.0030023
– volume: 514
  start-page: 759
  year: 1999
  ident: ref_15
  article-title: Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey bee Apis mellifera
  publication-title: J. Physiol.
  doi: 10.1111/j.1469-7793.1999.759ad.x
  contributor:
    fullname: Goldberg
– volume: 50
  start-page: 7218
  year: 2016
  ident: ref_51
  article-title: Honey bees’ behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field
  publication-title: Environ. Sci. Technol.
  doi: 10.1021/acs.est.6b02658
  contributor:
    fullname: Tison
– volume: 100
  start-page: 1188
  year: 2007
  ident: ref_107
  article-title: Changes in levels of juvenile hormone and molting hormone in larvae and adult females of Chilo suppressalis (Lepidoptera: Pyralidae) after imidacloprid applications to rice
  publication-title: J. Econ. Entomol.
  doi: 10.1603/0022-0493(2007)100[1188:CILOJH]2.0.CO;2
  contributor:
    fullname: Yu
– volume: 43
  start-page: 308
  year: 2012
  ident: ref_63
  article-title: Cellular physiology of olfactory learning in the honeybee brain
  publication-title: Apidologie
  doi: 10.1007/s13592-012-0135-z
  contributor:
    fullname: Himmelreich
– volume: 41
  start-page: 73
  year: 2010
  ident: ref_98
  article-title: Heat shock proteins and cell death in situ localisation in hypopharyngeal glands of honeybee (Apis mellifera carnica) workers after imidacloprid or coumaphos treatment
  publication-title: Apidologie
  doi: 10.1051/apido/2009051
  contributor:
    fullname: Gregorc
– ident: ref_7
  doi: 10.1371/journal.pone.0048838
– volume: 35
  start-page: 11
  year: 1950
  ident: ref_91
  article-title: The relation of cholinesterase activity to change in cell number with age in the brain of the adult worker honeybee
  publication-title: J. Cell. Comp. Physiol.
  doi: 10.1002/jcp.1030350103
  contributor:
    fullname: Rockstein
– ident: ref_19
  doi: 10.1007/978-94-007-2099-2
– volume: 48
  start-page: 635
  year: 2017
  ident: ref_35
  article-title: Toxicity of thiametoxam on in vitro reared honey bee brood
  publication-title: Apidologie
  doi: 10.1007/s13592-017-0506-6
  contributor:
    fullname: Grillone
– volume: 6
  start-page: 38110
  year: 2016
  ident: ref_71
  article-title: Neonicotinoid-induced impairment of odour coding in the honeybee
  publication-title: Sci. Rep.
  doi: 10.1038/srep38110
  contributor:
    fullname: Andrione
– volume: 683
  start-page: 97
  year: 2010
  ident: ref_18
  article-title: State of the art on insect nicotinic acetylcholine receptor function in learning and memory
  publication-title: Insect Nicotinic Acetylcholine Receptors
  doi: 10.1007/978-1-4419-6445-8_9
  contributor:
    fullname: Thany
– volume: 2
  start-page: 566
  year: 2010
  ident: ref_92
  article-title: Nutritional regulation of division of labor in honey bees: toward a systems biology perspective
  publication-title: Wiley Interdiscip. Rev. Syst. Biol. Med.
  doi: 10.1002/wsbm.73
  contributor:
    fullname: Ament
– volume: 30
  start-page: 65
  year: 1978
  ident: ref_1
  article-title: Cholinergic systems in non-nervous tissues
  publication-title: Pharmacol. Rev.
  contributor:
    fullname: Sastry
– volume: 86
  start-page: 164
  year: 2006
  ident: ref_70
  article-title: Involvement of alpha-bungarotoxin-sensitive nicotinic receptors in long-term memory formation in the honeybee (Apis mellifera)
  publication-title: Neurobiol. Learn. Mem.
  doi: 10.1016/j.nlm.2006.02.003
  contributor:
    fullname: Gauthier
– volume: 2
  start-page: 509
  year: 2011
  ident: ref_37
  article-title: Honey bee risk assessment: new approaches for in vitro larvae rearing and data analyses
  publication-title: Methods Ecol. Evol.
  doi: 10.1111/j.2041-210X.2011.00099.x
  contributor:
    fullname: Hendriksma
– ident: ref_102
  doi: 10.1177/0192623319877154
– volume: 45
  start-page: 247
  year: 2005
  ident: ref_66
  article-title: Neonicotinoid insecticide toxicology: mechanisms of selective action
  publication-title: Annu. Rev. Pharmacol. Toxicol.
  doi: 10.1146/annurev.pharmtox.45.120403.095930
  contributor:
    fullname: Tomizawa
– volume: 521
  start-page: 77
  year: 2015
  ident: ref_44
  article-title: Seed coating with a neonicotinoid insecticide negatively affects wild bees
  publication-title: Nature
  doi: 10.1038/nature14420
  contributor:
    fullname: Andersson
– volume: 16
  start-page: 119
  year: 2014
  ident: ref_42
  article-title: Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success
  publication-title: Agric. For. Entomol.
  doi: 10.1111/afe.12041
  contributor:
    fullname: Sandrock
– volume: 4
  start-page: 5566
  year: 2015
  ident: ref_41
  article-title: Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites
  publication-title: Sci. Rep.
  doi: 10.1038/srep05566
  contributor:
    fullname: Rondeau
– volume: 6
  start-page: 29608
  year: 2016
  ident: ref_114
  article-title: Neonicotinoid-contaminated pollinator strips adjacent to cropland reduce honey bee nutritional status
  publication-title: Sci. Rep.
  doi: 10.1038/srep29608
  contributor:
    fullname: Mogren
– volume: 15
  start-page: 615
  year: 2006
  ident: ref_113
  article-title: A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee
  publication-title: Insect Mol. Biol.
  doi: 10.1111/j.1365-2583.2006.00672.x
  contributor:
    fullname: Claudianos
– volume: 70
  start-page: 3231
  year: 2013
  ident: ref_72
  article-title: Two types of muscarinic acetylcholine receptors in Drosophila and other arthropods
  publication-title: Cell. Mol. Life Sci.
  doi: 10.1007/s00018-013-1334-0
  contributor:
    fullname: Collin
– ident: ref_13
  doi: 10.1101/105700
– volume: 51
  start-page: 1727
  year: 2017
  ident: ref_46
  article-title: The neonicotinoid insecticide thiacloprid impacts upon bumblebee colony development under field conditions
  publication-title: Environ. Sci. Technol.
  doi: 10.1021/acs.est.6b04791
  contributor:
    fullname: Ellis
– volume: 9
  start-page: 1
  year: 2014
  ident: ref_50
  article-title: Neonicotinoids interfere with specific components of naviagtion in honeybees
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0091364
  contributor:
    fullname: Fischer
– ident: ref_86
  doi: 10.1371/journal.pone.0014720
– ident: ref_99
  doi: 10.1371/journal.pone.0171529
– volume: 243
  start-page: 1588
  year: 2018
  ident: ref_103
  article-title: Endocrine disruption and chronic effects of plant protection products in bees: Can we better protect our pollinators?
  publication-title: Environ. Pollut.
  doi: 10.1016/j.envpol.2018.09.117
  contributor:
    fullname: Christen
– volume: 49
  start-page: 215
  year: 2002
  ident: ref_108
  article-title: Cholinergic regulation of the corpora allata in adult male loreyi leafworm Mythimna loreyi
  publication-title: Arch. Insect Biochem. Physiol.
  doi: 10.1002/arch.10022
  contributor:
    fullname: Kou
– volume: 52
  start-page: 9464
  year: 2013
  ident: ref_68
  article-title: Nicotinic acetylcholine receptor agonists: a milestone for modern crop protection
  publication-title: Angew. Chemie Int. Ed.
  doi: 10.1002/anie.201302550
  contributor:
    fullname: Jeschke
– volume: 78
  start-page: 83
  year: 2004
  ident: ref_53
  article-title: Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.)
  publication-title: Elsevier
  contributor:
    fullname: Decourtye
– volume: 71
  start-page: 177
  year: 2014
  ident: ref_112
  article-title: Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera)
  publication-title: J. Insect Physiol.
  doi: 10.1016/j.jinsphys.2014.10.002
  contributor:
    fullname: Schmehl
– volume: 22
  start-page: 467
  year: 2013
  ident: ref_17
  article-title: Cellular Mechanisms of Neuronal Plasticity in the Honeybee Brain
  publication-title: Handb. Behav. Neurosci.
  doi: 10.1016/B978-0-12-415823-8.00035-6
– volume: 147
  start-page: 200
  year: 2018
  ident: ref_52
  article-title: Assessment of acute sublethal effects of clothianidin on motor function of honeybee workers using video-tracking analysis
  publication-title: Ecotoxicol. Environ. Saf.
  doi: 10.1016/j.ecoenv.2017.08.047
  contributor:
    fullname: Alkassab
– volume: 533
  start-page: 132
  year: 1990
  ident: ref_65
  article-title: Sensitive nicotinic and mixed nicotinic-muscarinic receptors in insect neurosecretory cells
  publication-title: Brain Res.
  doi: 10.1016/0006-8993(90)91805-Q
  contributor:
    fullname: Lapied
– ident: ref_110
  doi: 10.1371/journal.pone.0068191
– volume: 101
  start-page: 784
  year: 2008
  ident: ref_87
  article-title: Lethal and sublethal effects of imidacloprid on Osmia lignaria and clothianidin on Megachile rotundata (Hymenoptera: Megachilidae)
  publication-title: J. Econ. Entomol.
  doi: 10.1603/0022-0493(2008)101[784:LASEOI]2.0.CO;2
  contributor:
    fullname: Abbott
– volume: 69
  start-page: 161
  year: 1981
  ident: ref_78
  article-title: The acetylcholine contents of honeys from different bees as determined in four-point-assays
  publication-title: Comp. Biochem. Physiol. Part C Comp. Pharmacol.
  doi: 10.1016/0306-4492(81)90121-0
  contributor:
    fullname: Valente
– volume: 81
  start-page: 215
  year: 1996
  ident: ref_69
  article-title: Mecamylamine-induced impairment of acquisition and retrieval of olfactory conditioning in the honeybee
  publication-title: Behav. Brain Res.
  doi: 10.1016/S0166-4328(96)89081-4
  contributor:
    fullname: Lozano
– volume: 13
  start-page: 328
  year: 1982
  ident: ref_89
  article-title: Tracer experiments on the passage of insecticides through nurse bees as a basis for determining intoxication routes in honeybee larvae
  publication-title: Apidologie
  contributor:
    fullname: Wittmann
– volume: 25
  start-page: 362
  year: 2016
  ident: ref_73
  article-title: A new family of insect muscarinic acetylcholine receptors
  publication-title: Insect Mol. Biol.
  doi: 10.1111/imb.12229
  contributor:
    fullname: Xia
– ident: ref_83
  doi: 10.1371/journal.pone.0049472
– volume: 7
  start-page: 1
  year: 2017
  ident: ref_104
  article-title: Neonicotinoids act like endocrine disrupting chemicals in newly-emerged bees and winter bees
  publication-title: Sci. Rep.
  doi: 10.1038/s41598-017-10489-6
  contributor:
    fullname: Baines
– volume: 50
  start-page: 4071
  year: 2016
  ident: ref_109
  article-title: Molecular effects of neonicotinoids in honey bees (Apis mellifera)
  publication-title: Environ. Sci. Technol.
  doi: 10.1021/acs.est.6b00678
  contributor:
    fullname: Christen
– volume: 37
  start-page: 803
  year: 1959
  ident: ref_79
  article-title: Studies in the mode of action of royal jelly in honeybee development: II. Respiration of newly emerged larvae on various substrates
  publication-title: Can. J. Zool.
  doi: 10.1139/z59-081
  contributor:
    fullname: Shuel
– volume: 69
  start-page: 439
  year: 2019
  ident: ref_48
  article-title: Repellency of insecticides and the effect of thiacloprid on bumble bee colony development in red clover (Trifolium pratense L.) seed crops
  publication-title: Acta Agric. Scand. Sect. B Soil Plant Sci.
  contributor:
    fullname: Havstad
– volume: 16
  start-page: 1422
  year: 2006
  ident: ref_61
  article-title: The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera
  publication-title: Genome Res.
  doi: 10.1101/gr.4549206
  contributor:
    fullname: Jones
– volume: 25
  start-page: 1648
  year: 2016
  ident: ref_45
  article-title: Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in Northern Germany: effects on honey bees (Apis mellifera)
  publication-title: Ecotoxicology
  doi: 10.1007/s10646-016-1725-8
  contributor:
    fullname: Rolke
– volume: 4
  start-page: 1634
  year: 2013
  ident: ref_34
  article-title: Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms2648
  contributor:
    fullname: Palmer
– volume: 106
  start-page: 1604
  year: 2011
  ident: ref_23
  article-title: Expression patterns of nicotinic subunits α2, α7, α8, and β1 affect the kinetics and pharmacology of ACh-induced currents in adult bee olfactory neuropiles
  publication-title: J. Neurophysiol.
  doi: 10.1152/jn.00126.2011
  contributor:
    fullname: Dupuis
– volume: 683
  start-page: 25
  year: 2010
  ident: ref_26
  article-title: Diversity of insect nicotinic acetylcholine receptor subunits
  publication-title: Adv. Exp. Med. Biol.
  doi: 10.1007/978-1-4419-6445-8_3
  contributor:
    fullname: Jones
– volume: 274
  start-page: 95
  year: 1999
  ident: ref_16
  article-title: Separation of voltage- and ligand-gated calcium influx in locust neurons by optical imaging
  publication-title: Neurosci. Lett.
  doi: 10.1016/S0304-3940(99)00694-1
  contributor:
    fullname: Oertner
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Snippet Acetylcholine (ACh) is the major excitatory neurotransmitter in the insect central nervous system (CNS). However, besides the neuronal expression of ACh...
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SubjectTerms Acetylcholine
Acetylcholine receptors (nicotinic)
Bees
Behavior
Central nervous system
Cholinergic transmission
Cholinergics
Developmental stages
Food
Gene expression
Hypopharyngeal gland
Insecticides
Insects
Larval development
Livestock
Nervous system
Neurons
Neurotransmitters
Permeability
Pesticides
Pharmacology
Plant protection
Receptors
Review
Royal jelly
Signal transduction
Vertebrates
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Title Acetylcholine and Its Receptors in Honeybees: Involvement in Development and Impairments by Neonicotinoids
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