title: Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure.
abstract: BACKGROUND
  Honeybees provide economically and ecologically vital pollination services to crops and wild plants. During the last decade elevated colony losses have been documented in Europe and North America. Despite growing consensus on the involvement of multiple causal factors, the underlying interactions impacting on honeybee health and colony failure are not fully resolved. Parasites and pathogens are among the main candidates, but sublethal exposure to widespread agricultural pesticides may also affect bees.
  
  
  RESULTS
  To investigate effects of sublethal dietary neonicotinoid exposure on honeybee colony performance, a fully crossed experimental design was implemented using 24 colonies, including sister-queens from two different strains, and experimental in-hive pollen feeding with or without environmentally relevant concentrations of thiamethoxam and clothianidin. Honeybee colonies chronically exposed to both neonicotinoids over two brood cycles exhibited decreased performance in the short-term resulting in declining numbers of adult bees (-28%) and brood (-13%), as well as a reduction in honey production (-29%) and pollen collections (-19%), but colonies recovered in the medium-term and overwintered successfully. However, significantly decelerated growth of neonicotinoid-exposed colonies during the following spring was associated with queen failure, revealing previously undocumented long-term impacts of neonicotinoids: queen supersedure was observed for 60% of the neonicotinoid-exposed colonies within a one year period, but not for control colonies. Linked to this, neonicotinoid exposure was significantly associated with a reduced propensity to swarm during the next spring. Both short-term and long-term effects of neonicotinoids on colony performance were significantly influenced by the honeybees' genetic background.
  
  
  CONCLUSIONS
  Sublethal neonicotinoid exposure did not provoke increased winter losses. Yet, significant detrimental short and long-term impacts on colony performance and queen fate suggest that neonicotinoids may contribute to colony weakening in a complex manner. Further, we highlight the importance of the genetic basis of neonicotinoid susceptibility in honeybees which can vary substantially.
authors.affiliation: Agroscope, Swiss Bee Research Centre, Berne, Switzerland.
authors.forename: Christoph
authors.initials: C
authors.lastname: Sandrock
authors.affiliation: Seminar for Statistics, ETH Zurich, Zurich, Switzerland.
authors.forename: Matteo
authors.initials: M
authors.lastname: Tanadini
authors.affiliation: Division of Biostatistics, Institute for Social and Preventive Medicine, University of Zurich, Zurich, Switzerland.
authors.forename: Lorenzo G
authors.initials: LG
authors.lastname: Tanadini
authors.affiliation: Agroscope, Swiss Bee Research Centre, Berne, Switzerland; Institute of Bee Health, Vetsuisse Faculty, University of Berne, Berne, Switzerland.
authors.forename: Aline
authors.initials: A
authors.lastname: Fauser-Misslin
authors.affiliation: School of Agriculture, Policy and Development, University of Reading, Reading, United Kingdom.
authors.forename: Simon G
authors.initials: SG
authors.lastname: Potts
authors.affiliation: Agroscope, Swiss Bee Research Centre, Berne, Switzerland; Institute of Bee Health, Vetsuisse Faculty, University of Berne, Berne, Switzerland.
authors.forename: Peter
authors.initials: P
authors.lastname: Neumann
mesh_terms: D000821:Animal Feed; D000818:Animals; D001516:Bees / Q000187:drug effects* / Q000502:physiology*; D004781:Environmental Exposure / Q000009:adverse effects*; D010575:Pesticides / Q000009:adverse effects*
chemical_list: D010575:Pesticides
references.citation: Pest Manag Sci. 2008 Nov;64(11):1099-105
references.pmid: 18561166
references.citation: Pest Manag Sci. 2004 Mar;60(3):291-6
references.pmid: 15025241
references.citation: PLoS Biol. 2006 Jan;4(1):e1
references.pmid: 16332160
references.citation: PLoS One. 2011 Feb 23;6(2):e14720
references.pmid: 21373182
references.citation: J Econ Entomol. 2009 Apr;102(2):474-9
references.pmid: 19449624
references.citation: Curr Biol. 2009 Jun 9;19(11):915-8
references.pmid: 19427214
references.citation: Science. 2012 Apr 20;336(6079):351-2
references.pmid: 22461500
references.citation: Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):14790-5
references.pmid: 19706391
references.citation: Annu Rev Entomol. 2007;52:81-106
references.pmid: 16842032
references.citation: PLoS One. 2011;6(11):e26796
references.pmid: 22073195
references.citation: PLoS One. 2012;7(4):e35954
references.pmid: 22563427
references.citation: PLoS One. 2014 Apr 09;9(4):e94482
references.pmid: 24718419
references.citation: PLoS One. 2013 Oct 23;8(10):e77193
references.pmid: 24194871
references.citation: Environ Microbiol Rep. 2009 Apr;1(2):110-3
references.pmid: 23765741
references.citation: Annu Rev Entomol. 2008;53:191-208
references.pmid: 17803456
references.citation: J Insect Physiol. 2013 Jan;59(1):113-9
references.pmid: 23147024
references.citation: PLoS One. 2010 Oct 06;5(10):e13181
references.pmid: 20949138
references.citation: Proc Natl Acad Sci U S A. 2011 Jan 11;108(2):662-7
references.pmid: 21199943
references.citation: Biol Lett. 2010 Aug 23;6(4):562-5
references.pmid: 20089536
references.citation: Science. 2006 Apr 21;312(5772):431-3
references.pmid: 16627742
references.citation: PLoS One. 2014 Jan 08;9(1):e77547
references.pmid: 24416121
references.citation: J Econ Entomol. 2009 Apr;102(2):616-23
references.pmid: 19449641
references.citation: PLoS One. 2013 Jun 12;8(6):e66375
references.pmid: 23776667
references.citation: Environ Microbiol. 2009 Sep;11(9):2284-90
references.pmid: 19737304
references.citation: PLoS One. 2011 Apr 18;6(4):e18491
references.pmid: 21533156
references.citation: Environ Microbiol. 2010 Mar;12(3):774-82
references.pmid: 20050872
references.citation: PLoS One. 2012;7(11):e49472
references.pmid: 23166680
references.citation: Science. 2012 Jun 8;336(6086):1304-6
references.pmid: 22679096
references.citation: Ecotoxicology. 2011 Jan;20(1):149-57
references.pmid: 21080222
references.citation: J Exp Biol. 2012 Jun 15;215(Pt 12):2022-9
references.pmid: 22623190
references.citation: Ann Bot. 2009 Jun;103(9):1579-88
references.pmid: 19339297
references.citation: Nature. 2012 Nov 1;491(7422):105-8
references.pmid: 23086150
references.citation: J Exp Biol. 2013 May 15;216(Pt 10):1799-807
references.pmid: 23393272
references.citation: Nature. 2013 May 9;497(7448):188
references.pmid: 23657341
references.citation: Environ Microbiol Rep. 2013 Feb;5(1):17-29
references.pmid: 23757127
references.citation: J Invertebr Pathol. 2008 Jan;97(1):76-8
references.pmid: 17651750
references.citation: J Agric Food Chem. 2012 May 9;60(18):4449-56
references.pmid: 22452667
references.citation: Prev Vet Med. 2013 Feb 1;108(2-3):225-33
references.pmid: 22939774
references.citation: Proc Biol Sci. 2007 Feb 7;274(1608):303-13
references.pmid: 17164193
references.citation: Bull Environ Contam Toxicol. 2010 Sep;85(3):229-34
references.pmid: 20658226
references.citation: Ecol Lett. 2013 Dec;16(12):1463-9
references.pmid: 24112478
references.citation: Trends Pharmacol Sci. 2001 Nov;22(11):573-80
references.pmid: 11698101
references.citation: Insects. 2013 Jan 04;4(1):71-89
references.pmid: 26466796
references.citation: PLoS Pathog. 2012;8(6):e1002735
references.pmid: 22719246
references.citation: PLoS One. 2008;3(12):e4071
references.pmid: 19115015
references.citation: Biom J. 2008 Jun;50(3):346-63
references.pmid: 18481363
references.citation: PLoS One. 2012;7(8):e43562
references.pmid: 22927991
references.citation: Nature. 2013 Apr 25;496(7446):408
references.pmid: 23619669
references.citation: J Invertebr Pathol. 2010 Jan;103 Suppl 1:S96-119
references.pmid: 19909970
references.citation: Science. 2013 May 10;340(6133):674-6
references.pmid: 23661734
references.citation: Environ Toxicol Chem. 2001 Nov;20(11):2482-6
references.pmid: 11699773
references.citation: PLoS One. 2013;8(1):e54092
references.pmid: 23382869
references.citation: J Insect Physiol. 2008 Oct-Nov;54(10-11):1392-9
references.pmid: 18761014
references.citation: Trends Ecol Evol. 2010 Jun;25(6):345-53
references.pmid: 20188434
references.citation: Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):18466-71
references.pmid: 24145453
references.citation: Curr Biol. 2008 Oct 28;18(20):1572-5
references.pmid: 18926704
references.citation: PLoS One. 2009 Aug 03;4(8):e6481
references.pmid: 19649264
references.citation: Ecotoxicology. 2012 May;21(4):973-92
references.pmid: 22350105
references.citation: Ecotoxicol Environ Saf. 1999 Oct;44(2):147-53
references.pmid: 10571460
references.citation: Pest Manag Sci. 2001 Oct;57(10):906-13
references.pmid: 11695183
references.citation: PLoS One. 2014 Mar 19;9(3):e91364
references.pmid: 24646521
references.citation: Naturwissenschaften. 2012 Feb;99(2):153-8
references.pmid: 22246149
references.citation: Pest Manag Sci. 2005 Feb;61(2):111-25
references.pmid: 15619715
references.citation: Trends Microbiol. 2011 Dec;19(12):614-20
references.pmid: 22032828
references.citation: PLoS One. 2011;6(6):e21550
references.pmid: 21738706
references.citation: PLoS One. 2013 Nov 04;8(11):e79872
references.pmid: 24224015
references.citation: J Econ Entomol. 2007 Jun;100(3):765-72
references.pmid: 17598537
references.citation: Nature. 2012 Nov 1;491(7422):43-5
references.pmid: 23086148
references.citation: PLoS One. 2012;7(1):e30023
references.pmid: 22253863
references.citation: PLoS One. 2012;7(1):e29268
references.pmid: 22235278
references.citation: J Agric Food Chem. 2011 Apr 13;59(7):2897-908
references.pmid: 20565065
references.citation: Adv Exp Med Biol. 2010;683:85-95
references.pmid: 20737791
references.citation: Pest Manag Sci. 2012 Jun;68(6):819-27
references.pmid: 22488890
references.citation: BMC Genomics. 2011 Oct 10;12:496
references.pmid: 21985689
references.citation: Nat Commun. 2013;4:1634
references.pmid: 23535655
references.citation: Proc Natl Acad Sci U S A. 2011 Apr 5;108(14):5909-14
references.pmid: 21422295
references.citation: Environ Toxicol. 2014 Oct;29(10):1122-33
references.pmid: 23339138
references.citation: J Invertebr Pathol. 2012 Feb;109(2):175-82
references.pmid: 22206912
references.citation: J Econ Entomol. 2002 Feb;95(1):28-35
references.pmid: 11942761
references.citation: Science. 2007 Oct 12;318(5848):283-7
references.pmid: 17823314
references.citation: Proc Natl Acad Sci U S A. 2011 Aug 2;108(31):12657-62
references.pmid: 21775671
references.citation: Science. 2008 Feb 8;319(5864):724-5; author reply 724-5
references.pmid: 18258878
references.citation: PLoS One. 2014 Mar 19;9(3):e91686
references.pmid: 24646894
references.citation: Science. 2012 Apr 20;336(6079):348-50
references.pmid: 22461498
references.citation: Ecotoxicology. 2010 Nov;19(8):1612-9
references.pmid: 20872243
references.citation: Environ Microbiol. 2015 Apr;17(4):969-83
references.pmid: 25611325
references.citation: Insect Mol Biol. 2006 Oct;15(5):615-36
references.pmid: 17069637
references.citation: Toxicology. 2013 Jul 5;309:39-51
references.pmid: 23603429
references.citation: Proc Natl Acad Sci U S A. 2013 May 28;110(22):8842-6
references.pmid: 23630255
references.citation: PLoS One. 2013 Jul 02;8(7):e68191
references.pmid: 23844170
references.citation: PLoS One. 2012;7(2):e31051
references.pmid: 22319603
references.citation: PLoS One. 2010 Mar 19;5(3):e9754
references.pmid: 20333298
references.citation: Science. 2006 Jul 21;313(5785):351-4
references.pmid: 16857940