title: Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae.
abstract: Recent declines in honey bee populations and increasing demand for insect-pollinated crops raise concerns about pollinator shortages. Pesticide exposure and pathogens may interact to have strong negative effects on managed honey bee colonies. Such findings are of great concern given the large numbers and high levels of pesticides found in honey bee colonies. Thus it is crucial to determine how field-relevant combinations and loads of pesticides affect bee health. We collected pollen from bee hives in seven major crops to determine 1) what types of pesticides bees are exposed to when rented for pollination of various crops and 2) how field-relevant pesticide blends affect bees' susceptibility to the gut parasite Nosema ceranae. Our samples represent pollen collected by foragers for use by the colony, and do not necessarily indicate foragers' roles as pollinators. In blueberry, cranberry, cucumber, pumpkin and watermelon bees collected pollen almost exclusively from weeds and wildflowers during our sampling. Thus more attention must be paid to how honey bees are exposed to pesticides outside of the field in which they are placed. We detected 35 different pesticides in the sampled pollen, and found high fungicide loads. The insecticides esfenvalerate and phosmet were at a concentration higher than their median lethal dose in at least one pollen sample. While fungicides are typically seen as fairly safe for honey bees, we found an increased probability of Nosema infection in bees that consumed pollen with a higher fungicide load. Our results highlight a need for research on sub-lethal effects of fungicides and other chemicals that bees placed in an agricultural setting are exposed to.
authors.affiliation: Bee Research Laboratory, USDA-ARS, Beltsville, Maryland, United States of America.
authors.forename: Jeffery S
authors.initials: JS
authors.lastname: Pettis
authors.forename: Elinor M
authors.initials: EM
authors.lastname: Lichtenberg
authors.forename: Michael
authors.initials: M
authors.lastname: Andree
authors.forename: Jennie
authors.initials: J
authors.lastname: Stitzinger
authors.forename: Robyn
authors.initials: R
authors.lastname: Rose
authors.forename: Dennis
authors.initials: D
authors.lastname: Vanengelsdorp
mesh_terms: D000818:Animals; D001516:Bees / Q000187:drug effects* / Q000382:microbiology*; D004198:Disease Susceptibility / Q000139:chemically induced; D005659:Fungicides, Industrial / Q000633:toxicity; D016818:Nosema / Q000472:pathogenicity*; D010575:Pesticides / Q000633:toxicity*; D054817:Pollination
chemical_list: D005659:Fungicides, Industrial; D010575:Pesticides
references.citation: J Econ Entomol. 2006 Oct;99(5):1565-70
references.pmid: 17066783
references.citation: Environ Microbiol. 2008 Oct;10(10):2659-69
references.pmid: 18647336
references.citation: Proc Biol Sci. 2007 Feb 7;274(1608):303-13
references.pmid: 17164193
references.citation: PLoS One. 2012;7(8):e43562
references.pmid: 22927991
references.citation: PLoS One. 2013;8(1):e54092
references.pmid: 23382869
references.citation: Naturwissenschaften. 2012 Feb;99(2):153-8
references.pmid: 22246149
references.citation: J Econ Entomol. 2010 Oct;103(5):1517-23
references.pmid: 21061948
references.citation: J Econ Entomol. 2004 Jun;97(3):735-40
references.pmid: 15279245
references.citation: PLoS One. 2011 Feb 23;6(2):e14720
references.pmid: 21373182
references.citation: J Invertebr Pathol. 2012 Mar;109(3):326-9
references.pmid: 22285445
references.citation: Mol Ecol. 2010 Nov;19(21):4823-9
references.pmid: 20958818
references.citation: Pest Manag Sci. 2003 Mar;59(3):269-78
references.pmid: 12639043
references.citation: J Econ Entomol. 1947 Jun;40(3):333-8
references.pmid: 20264495
references.citation: Science. 2012 Apr 20;336(6079):351-2
references.pmid: 22461500
references.citation: PLoS One. 2012;7(6):e39114
references.pmid: 22761727
references.citation: J Insect Physiol. 2012 Aug;58(8):1042-9
references.pmid: 22497859
references.citation: Annu Rev Entomol. 2007;52:81-106
references.pmid: 16842032
references.citation: J Econ Entomol. 2006 Apr;99(2):253-62
references.pmid: 16686121
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: J Econ Entomol. 2006 Aug;99(4):1046-50
references.pmid: 16937654
references.citation: J Insect Physiol. 2012 May;58(5):613-20
references.pmid: 22212860
references.citation: Environ Microbiol. 2010 Mar;12(3):774-82
references.pmid: 20050872
references.citation: J Exp Biol. 2012 Jun 15;215(Pt 12):2022-9
references.pmid: 22623190
references.citation: J Invertebr Pathol. 2012 Sep 15;111(1):68-73
references.pmid: 22750047
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: Environ Monit Assess. 2008 Sep;144(1-3):143-50
references.pmid: 17952621
references.citation: J Agric Food Chem. 2012 May 9;60(18):4449-56
references.pmid: 22452667
references.citation: J Insect Physiol. 2012 Aug;58(8):1090-5
references.pmid: 22609362
references.citation: Ecotoxicology. 2012 Oct;21(7):1937-45
references.pmid: 22614036
references.citation: J Invertebr Pathol. 2010 Jan;103 Suppl 1:S80-95
references.pmid: 19909973
references.citation: Science. 2013 Mar 29;339(6127):1608-11
references.pmid: 23449997
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: Environ Entomol. 2007 Oct;36(5):1238-45
references.pmid: 18284749
references.citation: PLoS One. 2011;6(6):e21550
references.pmid: 21738706
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