Abstract
Honey bee (Apis mellifera L.) populations have been experiencing notable mortality in Europe and North America. No single cause has been identified for these dramatic losses, but rather multiple interacting factors are likely responsible (such as pesticides, malnutrition, habitat loss, and pathogens). Paraquat is one of the most widely used non-selective herbicides, especially in developing countries. This herbicide is considered slightly toxic to honey bees, despite being reported as a highly effective inducer of oxidative stress in a wide range of living systems. Here, we test the effects of paraquat on the expression of detoxification and antioxidant-related genes, as well as on the dynamics of pathogen titers. Moreover, we tested the effects of pollen as mitigating factor to paraquat exposure. Our results show significant changes in the expression of several antioxidant-related and detoxification-related genes in the presence of paraquat, as well as an increase of pathogens titers. Finally, we demonstrate a mitigating effect of pollen through the up-regulation of specific genes and improvement of survival of bees exposed to paraquat. The presence of pollen in the diet was also correlated with a reduced prevalence of Nosema and viral pathogens. We discuss the importance of honey bees’ nutrition, especially the availability of pollen, on colony losses chronically reported in the USA and Europe.
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References
Alaux C, Allier F, Decourtye A et al (2017) A “Landscape physiology” approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats. Sci Rep 7:40568. https://doi.org/10.1038/srep40568
Alaux C, Brunet J-L, Dussaubat C et al (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol 12:774–782. https://doi.org/10.1111/j.1462-2920.2009.02123.x
Alaux C, Dantec C, Parrinello H, Le Conte Y (2011) Nutrigenomics in honey bees: digital gene expression analysis of pollen’s nutritive effects on healthy and varroa-parasitized bees. BMC Genomics 12:496. https://doi.org/10.1186/1471-2164-12-496
Almaraz-Abarca N, da Graça Campos M, Ávila-Reyes JA et al (2007) Antioxidant activity of polyphenolic extract of monofloral honeybee-collected pollen from mesquite (Prosopis juliflora, Leguminosae). J Food Compos Anal 20:119–124. https://doi.org/10.1016/j.jfca.2006.08.001
Amdam GV, Norberg K, Fondrk MK, Page RE (2004) Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc Natl Acad Sci USA 101:11350–5. https://doi.org/10.1073/pnas.0403073101
Amdam GV, Norberg K, Hagen A, Omholt SW (2003) Social exploitation of vitellogenin. Proc Natl Acad Sci USA 100:1799–802. https://doi.org/10.1073/pnas.0333979100
Amiri E, Meixner M, Nielsen SL, Kryger P (2015) Four categories of viral infection describe the health status of honey bee colonies. PLoS ONE 10:e0140272. https://doi.org/10.1371/journal.pone.0140272
Angelova MB, Pashova SB, Spasova BK et al (2005) Oxidative stress response of filamentous fungi induced by hydrogen peroxide and paraquat. Mycol Res 109:150–158. https://doi.org/10.1017/S0953756204001352
Antúnez K, Martín-Hernández R, Prieto L et al (2009) Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ Microbiol 11:2284–2290. https://doi.org/10.1111/j.1462-2920.2009.01953.x
Basualdo M, Barragán S, Antúnez K (2014) Bee bread increases honeybee haemolymph protein and promote better survival despite of causing higher N osema ceranae abundance in honeybees. Environ Microbiol Rep 6:396–400. https://doi.org/10.1111/1758-2229.12169
Berenbaum MR (2002) Postgenomic chemical ecology: from genetic code to ecological interactions. J Chem Ecol 28:873–896
Boncristiani H, Underwood R, Schwarz R et al (2012) Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. J Insect Physiol 58:613–620. https://doi.org/10.1016/j.jinsphys.2011.12.011
Bowen-Walker P, Martin S, Gunn A (1999) The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J Invertebr Pathol 73:101–106. https://doi.org/10.1006/jipa.1998.4807
Boyd NS (2014) Pepper and tomato root uptake of paraquat and flumioxazin. Weed Technol 28:626–632. https://doi.org/10.1614/WT-D-13-00177.1
Brandt BW, Zwaan BJ, Beekman M et al (2005) Shuttling between species for pathways of lifespan regulation: a central role for the vitellogenin gene family? Bioessays 27:339–346. https://doi.org/10.1002/bies.20161
Campos MGR, Frigerio C, Lopes J, Bogdanov S (2010) What is the future of Bee-Pollen? J ApiProduct ApiMed Sci 2:131–144. https://doi.org/10.3896/IBRA.4.02.4.01
Chaimanee V, Chantawannakul P, Chen Y et al (2012) Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. J Insect Physiol 58:1090–1095. https://doi.org/10.1016/j.jinsphys.2012.04.016
Chakrabarti P, Rana S, Sarkar S et al (2015) Pesticide-induced oxidative stress in laboratory and field populations of native honey bees along intensive agricultural landscapes in two Eastern Indian states. Apidologie 46:107–129. https://doi.org/10.1007/s13592-014-0308-z
Chen C-YO, Milbury PE, Collins FW, Blumberg JB (2007) Avenanthramides are bioavailable and have antioxidant activity in humans after acute consumption of an enriched mixture from oats. J Nutr 137:1375–1382
Chen Q, Niu Y, Zhang R et al (2010) The toxic influence of paraquat on hippocampus of mice: Involvement of oxidative stress. Neurotoxicology 31:310–316. https://doi.org/10.1016/j.neuro.2010.02.006
Claudianos C, Ranson H, Johnson RM et al (2006) A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol 15:615–636. https://doi.org/10.1111/j.1365-2583.2006.00672.x
Clejan L, Cederbaum AI (1989) Synergistic interactions between NADPH-cytochrome P-450 reductase, paraquat, and iron in the generation of active oxygen radicals. Biochem Pharmacol 38:1779–1786
Cocenza DS, De Moraes MA, Beppu MM, Fraceto LF (2012) Use of biopolymeric membranes for adsorption of paraquat herbicide from water. Water Air Soil Pollut 223:3093–3104. https://doi.org/10.1007/s11270-012-1092-x
Collison E, Hird H, Cresswell J, Tyler C (2016) Interactive effects of pesticide exposure and pathogen infection on bee health - a critical analysis. Biol Rev 91:1006–1019. https://doi.org/10.1111/brv.12206
Corona M, Robinson GE (2006) Genes of the antioxidant system of the honey bee: annotation and phylogeny. Insect Mol Biol 15:687–701. https://doi.org/10.1111/j.1365-2583.2006.00695.x
Cousin M, Silva-Zacarin E, Kretzschmar A et al (2013) Size changes in honey bee larvae oenocytes induced by exposure to paraquat at very low concentrations. PLoS ONE. https://doi.org/10.1371/journal.pone.0065693
Cox-Foster DL, Conlan S, Holmes EC et al (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science (80-) 318:283–287. https://doi.org/10.1126/science.1146498
Crampon M, Copard Y, Favreau G et al (2014) Occurrence of 1,1′-dimethyl-4,4′-bipyridinium (Paraquat) in irrigated soil of the Lake Chad Basin, Niger. Environ Sci Pollut Res 21:10601–10613. https://doi.org/10.1007/s11356-014-3064-8
Crapo JD, Oury T, Rabouille C et al (1992) Copper,zinc superoxide dismutase is primarily a cytosolic protein in human cells. Proc Natl Acad Sci USA 89:10405–10409
Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:149–157. https://doi.org/10.1007/s10646-010-0566-0
Dainat B, Evans JD, Chen YP et al (2012) Predictive markers of honey bee colony collapse. PLoS ONE 7:e32151. https://doi.org/10.1371/journal.pone.0032151
Delaplane KS, Mayer DF (2000) Crop pollination by bees. CABI Publishing, New York
Desneux N, Decourtye A, Delpuech J-M (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
Di Pasquale G, Salignon M, Le Conte Y et al (2013) Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS ONE 8:1–13. https://doi.org/10.1371/journal.pone.0072016
Di Prisco G, Annoscia D, Margiotta M et al (2016) A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health. Proc Natl Acad Sci USA 113:3203–3208. doi:https://doi.org/10.1073/pnas.1523515113
Dinis-Oliveira RJ, Duarte JA, Sánchez-Navarro A et al (2008) Paraquat poisonings: mechanisms of lung toxicity, clinical features, and treatment. Crit Rev Toxicol 38:13–71. https://doi.org/10.1080/10408440701669959
du Rand EE, Smit S, Beukes M et al (2015) Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine. Nat Publ Gr 1–11. https://doi.org/10.1038/srep11779
Eiri DM, Suwannapong G, Endler M et al (2015) Nosema ceranae can infect honey bee larvae and Reduces subsequent adult longevity. PLoS ONE 10:e0126330. https://doi.org/10.1371/journal.pone.0126330
Ellis JD, Evans JD, Pettis J (2010) Colony losses, managed colony population decline, and colony collapse disorder in the United States. J Apic Res 49:134–136. https://doi.org/10.3896/IBRA.1.49.1.30
Erban T, Harant K, Hubalek M et al (2015) In-depth proteomic analysis of Varroa destructor: detection of DWV-complex, ABPV, VdMLV and honeybee proteins in the mite. Sci Rep 5:13907. https://doi.org/10.1038/srep13907
Evans J, Aronstein KA, Chen Y, Hetru C, Imler JL, Jiang H et al (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect. Mol. Biol. 15:645–656. https://doi.org/10.1111/j.1365-2583.2006.00682.x
FAO (2003) Specification and evaluations for agricultural pesticides. Paraquat dichloride, 1,1’-dimethyl-4,4’-bispyridinium dichloride.
Fernández M, Ibanez M, Pico Y, Manes J (1998) Spatial and temporal trends of paraquat, diquat, and difenzoquat contamination in water from marsh areas of the valencian community (Spain). Arch Environ Contam Toxicol 35:377–384
Feyereisen R (2012) In: Gilbert LI (ed) Insect Molecular Biology and Biochemistry. Elsevier, Amsterdam, p 236–316
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247. https://doi.org/10.1038/35041687
Fleming JC, Schmehl DR, Ellis JD et al (2015) Characterizing the Impact of commercial pollen substitute diets on the level of Nosema spp. in honey bees (Apis mellifera L.). PLoS ONE 10:e0132014. https://doi.org/10.1371/journal.pone.0132014
Forsgren E, Fries I (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet Parasitol 170:212–217. https://doi.org/10.1016/j.vetpar.2010.02.010
Fukushima T, Tanaka K, Lim H, Moriyama M (2002) Mechanism of cytotoxicity of paraquat. Environ Health Prev Med 7:89–94
Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821. https://doi.org/10.1016/j.ecolecon.2008.06.014
Gauthier L, Tentcheva D, Tournaire M et al (2007) Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique. Apidologie 38:426–435. https://doi.org/10.1051/apido:2007026
Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97. https://doi.org/10.1007/s00253-010-2573-8
Genersch E, Aubert M (2010) Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet Res 41:54. https://doi.org/10.1051/vetres/2010027
Genersch E, von der Ohe W, Kaatz H et al (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332–352. https://doi.org/10.1051/apido/2010014
Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105–108. https://doi.org/10.1038/nature11585
Gisder S, Aumeier P, Genersch E (2009) Deformed wing virus: replication and viral load in mites (Varroa destructor). J Gen Virol 90:463–467. https://doi.org/10.1099/vir.0.005579-0
Goblirsch M, Huang ZYZ-YZY, Spivak M et al (2013) Physiological and behavioral changes in honey bees (Apis mellifera) induced by Nosema ceranae infection. PLoS ONE 8:e58165. https://doi.org/10.1371/journal.pone.0058165
Gong Y, Diao Q (2017) Current knowledge of detoxification mechanisms of xenobiotic in honey bees. Ecotoxicology 26:1–12. https://doi.org/10.1007/s10646-016-1742-7
Goulson D, Nicholls E, Botias C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science (80-) 347:1255957–1255957. https://doi.org/10.1126/science.1255957
Gregorc A, Evans JD, Scharf M, Ellis JD (2012) Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor). J Insect Physiol 58:1042–1049. https://doi.org/10.1016/j.jinsphys.2012.03.015
Hayaoka T, Dauterman WC (1982) Induction of glutathione S-transferase by phenobarbital and pesticides in various house fly strains and its effect on toxicity. Pestic Biochem Physiol 17:113–119. https://doi.org/10.1016/0048-3575(82)90015-3
Henry M, Beguin M, Requier F et al (2012) A common pesticide decreases foraging success and survival in honey bees. Science (80-) 336:348–350. https://doi.org/10.1126/science.1215039
Higes M, Martín-Hernández R, Garrido-Bailón E et al (2008) Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. J Invertebr Pathol 97:76–78. https://doi.org/10.1016/j.jip.2007.06.002
Huang W-F, Solter LF (2013) Comparative development and tissue tropism of Nosema apis and Nosema ceranae. J Invertebr Pathol 113:35–41. https://doi.org/10.1016/j.jip.2013.01.001
Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Annu Rev Entomol 50:421–445. https://doi.org/10.1146/annurev.ento.50.071803.130409
Jack CJ, Uppala SS, Lucas HM, Sagili RR (2016) Effects of pollen dilution on infection of Nosema ceranae in honey bees. J Insect Physiol 87:12–19. https://doi.org/10.1016/j.jinsphys.2016.01.004
Jakoby WB (1985) Glutathione transferases: an overview. Methods Enzymol 113:495–499
Jarvis RM, Hughes SM, Ledgerwood EC (2012) Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells. Free Radic Biol Med 53:1522–1530. https://doi.org/10.1016/j.freeradbiomed.2012.08.001
Johnson RM (2014) Honey Bee Toxicology. Annu Rev Entomol 60:415–434. https://doi.org/10.1146/annurev-ento-011613-162005
Johnson RM, Ellis MD, Mullin CA, Frazier M (2010) Pesticides and honey bee toxicity – USA. Apidologie 41:312–331. https://doi.org/10.1051/apido/2010018
Klein A-M, Vaissière BE, Cane JH et al (2007) Importance of pollinators in changing landscapes for world crops. Proc Biol Sci 274:303–313. https://doi.org/10.1098/rspb.2006.3721
Koo H-N, Lee S-G, Yun S-H et al (2016) Comparative Analyses of Cu-Zn Superoxide Dismutase (SOD1) and Thioredoxin Reductase (TrxR) at the mRNA Level between Apis mellifera L. and Apis cerana F. (Hymenoptera: Apidae) Under Stress Conditions. J Insect Sci. https://doi.org/10.1093/jisesa/iev159
Kostaropoulos I, Papadopoulos AI, Metaxakis A et al (2001) Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochem Mol Biol 31:313–319
Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci 99:16812–16816. https://doi.org/10.1073/pnas.262413599
Kujoth GC, Hiona A, Pugh TD et al (2005) Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science (80-) 309:481–484. https://doi.org/10.1126/science.1112125
Lee K (1991) Glutathione S-transferase activities in phytophagous insects: induction and inhibition by plant phototoxins and phenols. Insect Biochem 21:353–361. https://doi.org/10.1016/0020-1790(91)90001-U
Li-Byarlay H, Huang MH, Simone-Finstrom M et al (2016) Honey bee (Apis mellifera) drones survive oxidative stress due to increased tolerance instead of avoidance or repair of oxidative damage. Exp Gerontol 83:15–21. https://doi.org/10.1016/j.exger.2016.07.003
Long EY, Krupke CH (2016) Non-cultivated plants present a season-long route of pesticide exposure for honey bees. Nat Commun 7:11629. https://doi.org/10.1038/ncomms11629
Manevich Y, Hutchens S, Tew KD, Townsend DM (2013) Allelic variants of glutathione S-transferase P1-1 differentially mediate the peroxidase function of peroxiredoxin VI and alter membrane lipid peroxidation. Free Radic Biol Med 54:62–70. https://doi.org/10.1016/j.freeradbiomed.2012.10.556
Mao W, Schuler Ma, Berenbaum MR (2013) Honey constituents up-regulate detoxi fi cation and immunity genes in the western honey bee Apis mellifera. Proc Natl Acad Sci 110:8842–8846. https://doi.org/10.1073/pnas.1303884110/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1303884110
Medrzycki P, Giffard H, Aupinel P et al (2013) Standard methods for toxicology research in Apis mellifera. J Apic Res 52:1–60. https://doi.org/10.3896/IBRA.1.52.4.14
Mello MO, Silva-Filho MC (2002) Plant-insect interactions: an evolutionary arms race between two distinct defense mechanisms. Brazilian J Plant Physiol 14:71–81. https://doi.org/10.1590/S1677-04202002000200001
Michaud S, Boncristiani HF, Gouw JW et al (2015) Response of the honey bee (Apis mellifera) proteome to Israeli acute paralysis virus (IAPV) infection. Can J Zool 93:711–720. https://doi.org/10.1139/cjz-2014-0181
Morimoto T, Kojima Y, Toki T et al (2011) The habitat disruption induces immune-suppression and oxidative stress in honey bees. Ecol Evol 1:201–217. https://doi.org/10.1002/ece3.21
Mullin CA, Frazier M, Frazier JL et al (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5:e9754. https://doi.org/10.1371/journal.pone.0009754
Münch D, Amdam GV, Wolschin F (2008) Ageing in a eusocial insect: molecular and physiological characteristics of life span plasticity in the honey bee. Funct Ecol 22:407–421. https://doi.org/10.1111/j.1365-2435.2008.01419.x
Nanseu-Njiki CP, Dedzo GK, Ngameni E (2010) Study of the removal of paraquat from aqueous solution by biosorption onto Ayous (Triplochiton schleroxylon) sawdust. J Hazard Mater 179:63–71. https://doi.org/10.1016/j.jhazmat.2010.02.058
Nazzi F, Brown SP, Annoscia D et al (2012) Synergistic Parasite-Pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 8:e1002735. https://doi.org/10.1371/journal.ppat.1002735
Neumeister L, Isenring R (2011) Paraquat: Unacceptable health risks for users. Zurich
Omnia MA, Nabila MA, Nadia RR (2014) BiochemicaI effects of propolis and bee pollen in experimentally induced hyperammonimia in rats. BENHA Vet Med J 27:8–24
Pettis JS, Lichtenberg EM, Andree M et al (2013) Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE 8:e70182. https://doi.org/10.1371/journal.pone.0070182
Poole LB, Hall A, Nelson KJ (2011) Overview of peroxiredoxins in oxidant defense and redox regulation. Curr Protoc Toxicol Chapter 7:Unit7.9. https://doi.org/10.1002/0471140856.tx0709s49
Porrini MP, Sarlo EG, Medici SK et al (2011) Nosema ceranae development in Apis mellifera: influence of diet and infective inoculum. J Apic Res 50:35–41. https://doi.org/10.3896/IBRA.1.50.1.04
Potts SG, Biesmeijer JC, Kremen C et al (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007
IM RAO, SWAMY PM, DAS VSR (1980) Interference of herbicides with photochemical activities of chloroplasts in six shrub species. Weed Res 20:147–152. https://doi.org/10.1111/j.1365-3180.1980.tb00060.x
SAS Institute Inc. (2007) JMP®, Pro v10.0. SAS Institute Inc., Cary, NC, 1989–2007
Schneider CW, Tautz J, Grünewald B, Fuchs S (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS ONE 7:e30023. https://doi.org/10.1371/journal.pone.0030023
Seehuus S-C, Norberg K, Gimsa U et al (2006) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc Natl Acad Sci U S A 103:962–967. https://doi.org/10.1073/pnas.0502681103
Simone-Finstrom M, Li-Byarlay H, Huang MH et al (2016) Migratory management and environmental conditions affect lifespan and oxidative stress in honey bees. Sci Rep 6:32023. https://doi.org/10.1038/srep32023
Simone M, Evans JD, Spivak M (2009) Resin collection and social immunity in honey bees. Evolution (NY) 63:3016–3022. https://doi.org/10.1111/j.1558-5646.2009.00772.x
Smith KM, Loh EH, Rostal MK et al (2013) Pathogens, pests, and economics: drivers of honey bee colony declines and losses. Ecohealth 10:434–445. https://doi.org/10.1007/s10393-013-0870-2
Smith ML (2012) The honey bee parasite nosema ceranae: transmissible via food exchange? Cit Smith ML PLoS ONE. https://doi.org/10.1371/journal.pone.0043319
Strachecka A, Olszewski K, Paleolog J et al (2014) Coenzyme Q10 treatments influence the lifespan and key biochemical resistance systems in the honeybee, Apis mellifera. Arch Insect Biochem Physiol 86:165–179. https://doi.org/10.1002/arch.21159
Talcott RE, Shu H, Wei ET (1979) Dissociation of microsomal oxygen reduction and lipid peroxidation with the electron acceptors, paraquat and menadione. Biochem Pharmacol 28:665–671. https://doi.org/10.1016/0006-2952(79)90152-7
Traver BE, Fell RD (2012) Low natural levels of nosema ceranae in Apis mellifera queens. J Invertebr Pathol 110:408–410. https://doi.org/10.1016/j.jip.2012.04.001
Vandesompele J, De Preter K, Pattyn F et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034
vanEngelsdorp D, Meixner MD (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J Invertebr Pathol 103:S80–S95. https://doi.org/10.1016/j.jip.2009.06.011
Wang H, Zhang S-W, Zeng Z-J, Yan W-Y (2014) Nutrition affects longevity and gene expression in honey bee (Apis mellifera) workers. Apidologie 45:618–625. https://doi.org/10.1007/s13592-014-0276-3
Weirich GF, Collins AM, Williams VP (2002) Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie 33:3–14. https://doi.org/10.1051/apido:2001001
WHO (1984) Paraquat and diquat / published under the joint sponsorship of the United Nations Environment Programme, the International Labour Organisation, and the World Health Organization. World Health Organization, Geneva, p 181. https://www.who.int/iris/handle/10665/37301
Wilfert L, Long G, Leggett HC et al (2016) Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science (80-) 351:594–597. https://doi.org/10.1126/science.aac9976
Williams GR, Alaux C, Costa C et al (2013) Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. J Apic Res 52:1–36. https://doi.org/10.3896/IBRA.1.52.1.04
Winfree R, Aguilar R, Vázquez DP et al (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076. https://doi.org/10.1890/08-1245.1
Winston ML (1991) The biology of the honey bee. Harvard UP, Cambridge, MA
Zhang G, Zhang W, Cui X, Xu B (2015) Zinc nutrition increases the antioxidant defenses of honey bees. Entomol Exp Appl 156:201–210. https://doi.org/10.1111/eea.12342
Acknowledgements
This research was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES, as well as USDA-APHIS grant 14-8130-0360-CA. We thank Jennifer Keller for her technical support in the field.
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de Mattos, I.M., Soares, A.E.E. & Tarpy, D.R. Mitigating effects of pollen during paraquat exposure on gene expression and pathogen prevalence in Apis mellifera L. Ecotoxicology 27, 32–44 (2018). https://doi.org/10.1007/s10646-017-1868-2
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DOI: https://doi.org/10.1007/s10646-017-1868-2