Insecticides are chemicals used to kill insects, so it is unsurprising that many insecticides have the potential to harm honey bees (). However, bees are exposed to a great variety of other potentially toxic chemicals, including flavonoids and alkaloids that are produced by plants; mycotoxins produced by fungi; antimicrobials and acaricides that are introduced by beekeepers; and fungicides, herbicides, and other environmental contaminants. Although often regarded as uniquely sensitive to toxic compounds, honey bees are adapted to tolerate and even thrive in the presence of toxic compounds that occur naturally in their environment. The harm caused by exposure to a particular concentration of a toxic compound may depend on the level of simultaneous exposure to other compounds, pathogen levels, nutritional status, and a host of other factors. This review takes a holistic view of bee toxicology by taking into account the spectrum of xenobiotics to which bees are exposed.


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Literature Cited

  1. Alaux C, Brunet J-L, Dussaubat C, Mondet F, Tchamitchan S. 1.  et al. 2010. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12:3774–82 [Google Scholar]
  2. Aliano NP, Ellis MD. 2.  2008. Bee-to-bee contact drives oxalic acid distribution in honey bee colonies. Apidologie 39:5481–87 [Google Scholar]
  3. Anderson LD, Atkins EL. 3.  1968. Pesticide usage in relation to beekeeping. Annu. Rev. Entomol. 13:1213–38 [Google Scholar]
  4. Atkins EL, Anderson LD. 4.  1962. DDT resistance in honey bees. J. Econ. Entomol. 55:5791–92 [Google Scholar]
  5. Atkins EL, Kellum D. 5.  1986. Comparative morphogenic and toxicity studies on the effect of pesticides on honey bee brood. J. Apic. Res. 25:4242–55 [Google Scholar]
  6. Ayestaran A, Giurfa M, de Brito Sanchez MG. 6.  2010. Toxic but drank: gustatory aversive compounds induce post-ingestional malaise in harnessed honeybees. PLOS ONE 5:10e15000 [Google Scholar]
  7. Barbara GS, Zube C, Rybak J, Gauthier M, Grünewald B. 7.  2005. Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera. J. Comp. Physiol. A 191:9823–36 [Google Scholar]
  8. Barker RJ. 8.  1977. Some carbohydrates found in pollen and pollen substitutes are toxic to honey bees. J. Nutr. 107:101859–62 [Google Scholar]
  9. Barker RJ, Lehner Y. 9.  1974. Acceptance and sustenance value of naturally occurring sugars fed to newly emerged adult workers of honey bees (Apis mellifera L.). J. Exp. Zool. 187:2277–85 [Google Scholar]
  10. Barnett EA, Charlton AJ, Fletcher MR. 10.  2007. Incidents of bee poisoning with pesticides in the United Kingdom, 1994–2003. Pest Manag. Sci. 63:111051–57 [Google Scholar]
  11. Basedow T, El-Shafie HAF, Al-Ajlan AM, Abo-El-Saad MM. 11.  2012. Evaluation of Bacillus thuringiensis aizawai and neem for controlling the larvae of the greater wax moth, Galleria mellonella (Lepidoptera: Pyralidae). Int. J. Agric. Biol. 14:4629–32 [Google Scholar]
  12. Belzunces LP, Tchamitchian S, Brunet J-L. 12.  2012. Neural effects of insecticides in the honey bee. Apidologie 43:3348–70 [Google Scholar]
  13. Bernal J, Garrido-Bailón E, del Nozal MJ, González-Porto AV, Martín-Hernández R. 13.  et al. 2010. Overview of pesticide residues in stored pollen and their potential effect on bee colony (Apis mellifera) losses in Spain. J. Econ. Entomol. 103:61964–71 [Google Scholar]
  14. Berry JA, Hood WM, Pietravalle S, Delaplane KS. 14.  2013. Field-level sublethal effects of approved bee hive chemicals on honey bees (Apis mellifera L). PLOS ONE 8:10e76536 [Google Scholar]
  15. Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappalà L, Desneux N. 15.  2012. The non-target impact of spinosyns on beneficial arthropods. Pest Manag. Sci. 68:121523–36 [Google Scholar]
  16. Bogdanov S, Kilchenmann V, Imdorf A. 16.  1998. Acaricide residues in some bee products. J. Apic. Res. 37:257–67 [Google Scholar]
  17. Boppre M, Colegate SM, Edgar JA. 17.  2005. Pyrrolizidine alkaloids of Echium vulgare honey found in pure pollen. J. Agric. Food Chem. 53:3594–600 [Google Scholar]
  18. Bravo A, Likitvivatanavong S, Gill SS, Soberón M. 18.  2011. Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem. Mol. Biol. 41:7423–31 [Google Scholar]
  19. Bromenshenk JJ, Carlson SR, Simpson JC, Thomas JM. 19.  1985. Pollution monitoring of Puget Sound with honey bees. Science 227:4687632–34 [Google Scholar]
  20. Bromenshenk JJ, Gudatis JL, Carlson SR, Thomas JM, Simmons MA. 20.  1991. Population dynamics of honey bee nucleus colonies exposed to industrial pollutants. Apidologie 22:4359–69Effect of toxic metals in the environment on whole colonies. [Google Scholar]
  21. Brunet J-L, Badiou A, Belzunces LP. 21.  2005. In vivo metabolic fate of [14C]-acetamiprid in six biological compartments of the honeybee, Apis mellifera L. Pest Manag. Sci. 61:8742–48 [Google Scholar]
  22. Burdock GA. 22.  1998. Review of the biological properties and toxicity of bee propolis (propolis). Food Chem. Toxicol. 36:4347–63 [Google Scholar]
  23. Camp HB, Fukuto TR, Metcalf RL. 23.  1969. Toxicity of isopropyl parathion: effect of structure on toxicity and anticholinesterase activity. J. Agric. Food Chem. 17:2243–48 [Google Scholar]
  24. Casida JE, Durkin KA. 24.  2013. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu. Rev. Entomol. 58:99–117Explanation of insecticide modes of action. [Google Scholar]
  25. Charpentier G, Vidau C, Ferdy J-B, Tabart J, Vetillard A. 25.  2014. Lethal and sub-lethal effects of thymol on honeybee (Apis mellifera) larvae reared in vitro. Pest Manag. Sci. 70:1140–47 [Google Scholar]
  26. Chauzat M-P, Faucon J-P. 26.  2007. Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in France. Pest Manag. Sci. 63:111100–6 [Google Scholar]
  27. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA. 27.  et al. 2006. A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol. Biol. 15:5615–36 [Google Scholar]
  28. Collet C, Belzunces L. 28.  2007. Excitable properties of adult skeletal muscle fibres from the honeybee Apis mellifera. J. Exp. Biol. 210:3454–64 [Google Scholar]
  29. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y. 29.  et al. 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc. Natl. Acad. Sci. USA 104:177128–33 [Google Scholar]
  30. Cousin M, Silva-Zacarin E, Kretzschmar A, El Maataoui M, Brunet J-L, Belzunces LP. 30.  2013. Size changes in honey bee larvae oenocytes induced by exposure to paraquat at very low concentrations. PLOS ONE 8:5e65693 [Google Scholar]
  31. Couvillon MJ, Schürch R, Ratnieks FLW. 31.  2014. Dancing bees communicate a foraging preference for rural lands in high-level agri-environment schemes. Curr. Biology 24:111212–15 [Google Scholar]
  32. Cresswell J. 32.  2011. A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:1149–57Relationship between field dose of imidacloprid and effects studies. [Google Scholar]
  33. Dahlgren L, Johnson RM, Siegfried BD, Ellis MD. 33.  2012. Comparative toxicity of acaricides to honey bee (Hymenoptera: Apidae) workers and queens. J. Econ. Entomol. 105:61895–902 [Google Scholar]
  34. Desneux N, Decourtye A, Delpuech JM. 34.  2007. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52:81–106 [Google Scholar]
  35. Detzel A, Wink M. 35.  1993. Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4:18–18Repellence and toxicity for 63 toxins in nectar and pollen. [Google Scholar]
  36. Dewick PM. 36.  2009. Medicinal Natural Products: A Biosynthetic Approach Chichester, UK: Wiley, 3rd ed.. [Google Scholar]
  37. Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E. 37.  et al. 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc. Natl. Acad. Sci. USA 110:4618466–71 [Google Scholar]
  38. Dinter A, Brugger KE, Frost NM, Woodward MD. 38.  2009. Chlorantraniliprole (Rynaxypyr): a novel DuPontTM insecticide with low toxicity and low risk for honey bees (Apis mellifera) and bumble bees (Bombus terrestris) providing excellent tools for uses in integrated pest management. Julius-Kühn-Archiv 423:84–96 [Google Scholar]
  39. Duan JJ, Marvier M, Huesing J, Dively G, Huang ZY. 39.  2008. A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLOS ONE 3:1e1415 [Google Scholar]
  40. Eiri DM, Nieh JC. 40.  2012. A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. J. Exp. Biol. 215:122022–29 [Google Scholar]
  41. Elzen PJ, Elzen GW, Rubink W. 41.  2003. Comparative susceptibility of European and Africanized honey bee (Hymenoptera: Apidae) ecotypes to several insecticide classes. Southwest. Entomol. 28:4255–60 [Google Scholar]
  42. Engel P, Martinson VG, Moran NA. 42.  2012. Functional diversity within the simple gut microbiota of the honey bee. Proc. Natl. Acad. Sci. USA 109:2711002–7 [Google Scholar]
  43. Floris I, Satta A, Cabras P, Garau VL, Angioni A. 43.  2004. Comparison between two thymol formulations in the control of Varroa destructor: effectiveness, persistence, and residues. J. Econ. Entomol. 97:2187–91 [Google Scholar]
  44. Forkpah C, Dixon LR, Fahrbach SE, Rueppell O. 44.  2014. Xenobiotic effects on intestinal stem cell proliferation in adult honey bee (Apis mellifera L.) workers. PLOS ONE 9:3e91180 [Google Scholar]
  45. Forster R. 45.  2009. Bee poisoning caused by insecticidal seed treatment of maize in Germany in 2008. Julius-Kühn-Archiv 423:126–31 [Google Scholar]
  46. Fries I. 46.  1991. Treatment of sealed honey bee brood with formic acid for control of Varroa jacobsoni. Am. Bee J. 131:313–14 [Google Scholar]
  47. Giovenazzo P, Dubreuil P. 47.  2011. Evaluation of spring organic treatments against Varroa destructor (Acari: Varroidae) in honey bee Apis mellifera (Hymenoptera: Apidae) colonies in eastern Canada. Exp. Appl. Acarol. 55:165–76 [Google Scholar]
  48. González G, Hinojo MJ, Mateo R, Medina A, Jiménez M. 48.  2005. Occurrence of mycotoxin producing fungi in bee pollen. Int. J. Food Microbiol. 105:11–9 [Google Scholar]
  49. Grdiša M, Carović-Stanko K, Kolak I, Šatović Z. 49.  2009. Morphological and biochemical diversity of Dalmatian pyrethrum (Tanacetum cinerariifolium (Trevir.) Sch. Bip.). Agric. Conspec. Sci. ACS 74:273–80 [Google Scholar]
  50. Gregorc A, Smodiš Škerl MI. 50.  2007. Toxicological and immunohistochemical testing of honeybees after oxalic acid and rotenone treatments. Apidologie 38:3296–305 [Google Scholar]
  51. Guez D. 51.  2013. A common pesticide decreases foraging success and survival in honey bees: questioning the ecological relevance. Front. Physiol. 4:37 [Google Scholar]
  52. Haarmann T, Spivak M, Weaver D, Weaver B, Glenn T. 52.  2002. Effects of fluvalinate and coumaphos on queen honey bees (Hymenoptera: Apidae) in two commercial queen rearing operations. J. Econ. Entomol. 95:128–35 [Google Scholar]
  53. Hardstone MC, Scott JG. 53.  2010. Is Apis mellifera more sensitive to insecticides than other insects?. Pest Manag. Sci. 66:111171–80Broad comparison of insecticide toxicity between bees and other insects. [Google Scholar]
  54. Harris JW, Woodring J, Harbo JR. 54.  1996. Effects of carbon dioxide on levels of biogenic amines in the brains of queenless worker and virgin queen honey bees (Apis mellifera). J. Apic. Res. 35:269–78 [Google Scholar]
  55. Hawthorne DJ, Dively GP. 55.  2011. Killing them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger honey bees. PLOS ONE 6:11e26796 [Google Scholar]
  56. Hendriksma HP, Küting M, Härtel S, Näther A, Dohrmann AB. 56.  et al. 2013. Effect of stacked insecticidal Cry proteins from maize pollen on nurse bees (Apis mellifera carnica) and their gut bacteria. PLOS ONE 8:3e59589 [Google Scholar]
  57. Henry M, Béguin M, Requier F, Rollin O, Odoux J-F. 57.  et al. 2012. A common pesticide decreases foraging success and survival in honey bees. Science 336:6079348–50Application of modeling to infer colony effect of sublethal exposure. [Google Scholar]
  58. Heylen K, Gobin B, Arckens L, Huybrechts R, Billen J. 58.  2011. The effects of four crop protection products on the morphology and ultrastructure of the hypopharyngeal gland of the European honeybee, Apis mellifera. Apidologie 42:1103–16 [Google Scholar]
  59. Hillier NK, Frost EH, Shutler D. 59.  2013. Fate of dermally applied miticides fluvalinate and amitraz within honey bee (Hymenoptera: Apidae) bodies. J. Econ. Entomol. 106:2558–65 [Google Scholar]
  60. Hladun KR, Kaftanoglu O, Parker DR, Tran KD, Trumble JT. 60.  2013. Effects of selenium on development, survival, and accumulation in the honeybee (Apis mellifera L.). Environ. Toxicol. Chem. 32:112584–92 [Google Scholar]
  61. Hladun KR, Parker DR, Tran KD, Trumble JT. 61.  2013. Effects of selenium accumulation on phytotoxicity, herbivory, and pollination ecology in radish (Raphanus sativus L.). Environ. Pollut. 172:70–75 [Google Scholar]
  62. Hong S, Pedersen PL. 62.  2008. ATP synthase and the actions of inhibitors utilized to study its roles in human health, disease, and other scientific areas. Microbiol. Mol. Biol. Rev. 72:4590–641 [Google Scholar]
  63. Hrassnigg N, Brodschneider R, Fleischmann PH, Crailsheim K. 63.  2005. Unlike nectar foragers, honeybee drones (Apis mellifera) are not able to utilize starch as fuel for flight. Apidologie 36:4547–57 [Google Scholar]
  64. Huang W-F, Solter LF, Yau PM, Imai BS. 64.  2013. Nosema ceranae escapes fumagillin control in honey bees. PLOS Pathog. 9:3e1003185 [Google Scholar]
  65. Iwasa T, Motoyama N, Ambrose J, Roe RM. 65.  2004. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot. 23:5371–78 [Google Scholar]
  66. Johansen CA. 66.  1977. Pesticides and pollinators. Annu. Rev. Entomol. 22:177–92 [Google Scholar]
  67. Johnson RM, Dahlgren L, Siegfried BD, Ellis MD. 67.  2013. Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLOS ONE 8:1e54092 [Google Scholar]
  68. Johnson RM, Ellis MD, Mullin CA, Frazier M. 68.  2010. Pesticides and honey bee toxicity—USA. Apidologie 41:3312–31 [Google Scholar]
  69. Johnson RM, Mao W, Pollock HS, Niu G, Schuler MA, Berenbaum MR. 69.  2012. Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PLOS ONE 7:2e31051 [Google Scholar]
  70. Johnson RM, Wen Z, Schuler MA, Berenbaum MR. 70.  2006. Mediation of pyrethroid insecticide toxicity to honey bees (Hymenoptera: Apidae) by cytochrome P450 monooxygenases. J. Econ. Entomol. 99:41046–50 [Google Scholar]
  71. Kadala A, Charreton M, Jakob I, Le Conte Y, Collet C. 71.  2011. A use-dependent sodium current modification induced by type I pyrethroid insecticides in honeybee antennal olfactory receptor neurons. Neurotoxicology 32:3320–30 [Google Scholar]
  72. Kalnins MA, Detroy BF. 72.  1984. The effect of wood preservative treatment of beehives on honey bees and hive products. J. Agric. Food Chem. 32:51176–80 [Google Scholar]
  73. Kezic N, Lucic D, Sulimanovic D. 73.  1992. Induction of mixed function oxidase activity in honey bee as a bioassay for detection of environmental xenobiotics. Apidologie 23:3217–23 [Google Scholar]
  74. Köehler A, Pirk CWW, Nicolson SW. 74.  2012. Honeybees and nectar nicotine: deterrence and reduced survival versus potential health benefits. J. Insect Physiol. 58:2286–92 [Google Scholar]
  75. Kozak PR, Currie RW. 75.  2011. Laboratory study on the effects of temperature and three ventilation rates on infestations of Varroa destructor in clusters of honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 104:61774–82 [Google Scholar]
  76. Kretschmar JA, Baumann TW. 76.  1999. Caffeine in citrus flowers. Phytochemistry 52:119–23 [Google Scholar]
  77. Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K. 77.  2012. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLOS ONE 7:1e29268 [Google Scholar]
  78. Larson JL, Redmond CT, Potter DA. 78.  2013. Assessing insecticide hazard to bumble bees foraging on flowering weeds in treated lawns. PLOS ONE 8:6e66375 [Google Scholar]
  79. LeBlanc BW, Eggleston G, Sammataro D, Cornett C, Dufault R. 79.  et al. 2009. Formation of hydroxymethylfurfural in domestic high-fructose corn syrup and its toxicity to the honey bee (Apis mellifera). J. Agric. Food Chem. 57:167369–76 [Google Scholar]
  80. Levot GW. 80.  2008. An insecticidal refuge trap to control adult small hive beetle Aethina tumida Murray (Coleoptera: Nitidulidae) in honey bee colonies. J. Apic. Res. 47:3222–28 [Google Scholar]
  81. Liu M-Y, Plapp FW. 81.  1992. Mechanism of formamidine synergism of pyrethroids. Pestic. Biochem. Physiol. 43:2134–40 [Google Scholar]
  82. Main AR, Headley JV, Peru KM, Michel NL, Cessna AJ, Morrissey CA. 82.  2014. Widespread use and frequent detection of neonicotinoid insecticides in wetlands of Canada's prairie pothole region. PLOS ONE 9:3e92821 [Google Scholar]
  83. Malone LA, Burgess EPJ. 83.  2009. Impact of genetically modified crops on pollinators. Environmental Impact of Genetically Modified Crops N Ferry, AMR Gatehouse 199–224 Oxfordshire, UK: CABI [Google Scholar]
  84. Mao W, Rupasinghe SG, Johnson RM, Zangerl AR, Schuler MA, Berenbaum MR. 84.  2009. Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comp. Biochem. Physiol. B 154:4427–34 [Google Scholar]
  85. Mao W, Schuler MA, Berenbaum MR. 85.  2011. CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proc. Natl. Acad. Sci. USA 108:12657–62 [Google Scholar]
  86. Mao W, Schuler MA, Berenbaum MR. 86.  2013. Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. Proc. Natl. Acad. Sci. USA 110:8842–46Honey, pollen, and propolis xenobiotics affect detoxification capacity. [Google Scholar]
  87. McIndoo NE. 87.  1926. Effects on Honeybees of Spraying Fruit Trees with Arsenicals Washington, DC: US Dep. Agric. [Google Scholar]
  88. McMartin K. 88.  2009. Are calcium oxalate crystals involved in the mechanism of acute renal failure in ethylene glycol poisoning?. Clin. Toxicol. 47:9859–69 [Google Scholar]
  89. Medrzycki P, Sgolastra F, Bortolotti L, Bogo G, Tosi S. 89.  et al. 2010. Influence of brood rearing temperature on honey bee development and susceptibility to poisoning by pesticides. J. Apic. Res. 49:152–59 [Google Scholar]
  90. Meled M, Thrasyvoulou A, Belzunces LP. 90.  1998. Seasonal variations in susceptibility of Apis mellifera to the synergistic action of prochloraz and deltamethrin. Environ. Toxicol. Chem. 17:122517–20 [Google Scholar]
  91. Mendelsohn M, Kough J, Vaituzis Z, Matthews K. 91.  2003. Are Bt crops safe?. Nat. Biotechnol 21:91003–9 [Google Scholar]
  92. Moffett JO, Morton HL, MacDonald RH. 92.  1972. Toxicity of some herbicidal sprays to honey bees. J. Econ. Entomol. 65:132–36 [Google Scholar]
  93. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R. 93.  et al. 2010. High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLOS ONE 5:3e9754 [Google Scholar]
  94. Mussen EC, Lopez JE, Peng CYS. 94.  2004. Effects of selected fungicides on growth and development of larval honey bees, Apis mellifera L. (Hymenoptera: Apidae). Environ. Entomol. 33:51151–54 [Google Scholar]
  95. Nauen R, Ebbinghaus-Kintscher U, Salgado VL, Kaussmann M. 95.  2003. Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pestic. Biochem. Physiol. 76:255–69 [Google Scholar]
  96. Nauen R, Ebbinghaus-Kintscher U, Schmuck R. 96.  2001. Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Manag. Sci. 57:7577–86 [Google Scholar]
  97. Nicolas G, Sillans D. 97.  1989. Immediate and latent effects of carbon dioxide on insects. Annu. Rev. Entomol. 34:97–116 [Google Scholar]
  98. Niu G, Johnson RM, Berenbaum MR. 98.  2011. Toxicity of mycotoxins to honeybees and its amelioration by propolis. Apidologie 42:179–87 [Google Scholar]
  99. Patil PB, Zeng Y, Coursey T, Houston P, Miller I, Chen S. 99.  2010. Isolation and characterization of a Nocardiopsis sp. from honeybee guts. FEMS Microbiol. Lett. 312:2110–18 [Google Scholar]
  100. Pawlikowski T. 100.  2010. Pollination activity of bees (Apoidea: Apiformes) visiting the flowers of Tilia cordata Mill. and Tilia tomentosa Moench in an urban environment. J. Apic. Sci. 54:273–79 [Google Scholar]
  101. Peng Y-SC, Mussen E, Fong A, Montague MA, Tyler T. 101.  1992. Effects of chlortetracycline of honey bee worker larvae reared in vitro. J. Invertebr. Pathol. 60:2127–33 [Google Scholar]
  102. Pettis JS, Lichtenberg EM, Andree M, Stitzinger J, Rose R, vanEngelsdorp D. 102.  2013. Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLOS ONE 8:7e70182 [Google Scholar]
  103. Pettis JS, vanEngelsdorp D, Johnson J, Dively G. 103.  2012. Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99:2153–58 [Google Scholar]
  104. Pilling ED, Jepson PC. 104.  1993. Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera). Pestic. Sci. 39:4293–97 [Google Scholar]
  105. Qi S, Casida JE. 105.  2013. Species differences in chlorantraniliprole and flubendiamide insecticide binding sites in the ryanodine receptor. Pestic. Biochem. Physiol. 107:3321–26 [Google Scholar]
  106. Ramirez-Romero R, Desneux N, Decourtye A, Chaffiol A, Pham-Delègue MH. 106.  2008. Does Cry1ab protein affect learning performances of the honey bee Apis mellifera L. (Hymenoptera, Apidae)?. Ecotoxicol. Environ. Saf. 70:2327–33 [Google Scholar]
  107. Ratnaike RN. 107.  2003. Acute and chronic arsenic toxicity. Postgrad. Med. J. 79:933391–96 [Google Scholar]
  108. Reinhard A, Janke M, von der Ohe W, Kempf M, Theuring C. 108.  et al. 2009. Feeding deterrence and detrimental effects of pyrrolizidine alkaloids fed to honey bees (Apis mellifera). J. Chem. Ecol. 35:91086–95 [Google Scholar]
  109. Reybroeck W, Daeseleire E, De Brabander HF, Herman L. 109.  2012. Antimicrobials in beekeeping. Vet. Microbiol. 158:1–21–11 [Google Scholar]
  110. Rindfleisch JK. 110.  1977. The use of nitrous oxide as an anesthetic for honey bees. Am. Bee J. 117:622 [Google Scholar]
  111. Robertson HM, Wanner KW. 111.  2006. The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res. 16:111395–403 [Google Scholar]
  112. Robinson GE. 112.  1987. Regulation of honey bee age polyethism by juvenile hormone. Behav. Ecol. Sociobiol. 20:5329–38 [Google Scholar]
  113. Rortais A, Arnold G, Halm M-P, Touffet-Briens F. 113.  2005. Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36:171–83 [Google Scholar]
  114. Rose R, Dively G, Pettis J. 114.  2007. Effects of Bt corn pollen on honey bees: emphasis on protocol development. Apidologie 38:4368–77 [Google Scholar]
  115. Sammataro D, Weiss M. 115.  2013. Comparison of productivity of colonies of honey bees, Apis mellifera, supplemented with sucrose or high fructose corn syrup. J. Insect Sci. 13:191–13 [Google Scholar]
  116. Schmuck R, Stadler T, Schmidt HW. 116.  2003. Field relevance of a synergistic effect observed in the laboratory between an EBI fungicide and a chloronicotinyl insecticide in the honeybee (Apis mellifera L., Hymenoptera). Pest Manag. Sci. 59:3279–86 [Google Scholar]
  117. Schneider CW, Tautz J, Grünewald B, Fuchs S. 117.  2012. RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLOS ONE 7:1e30023 [Google Scholar]
  118. Schneider S, Eisenhardt D, Rademacher E. 118.  2012. Sublethal effects of oxalic acid on Apis mellifera (Hymenoptera: Apidae): changes in behaviour and longevity. Apidologie 43:2218–25 [Google Scholar]
  119. Schulz DJ, Robinson GE. 119.  2001. Octopamine influences division of labor in honey bee colonies. J. Comp. Physiol. A 187:153–61 [Google Scholar]
  120. Seehuus S-C, Norberg K, Gimsa U, Krekling T, Amdam GV. 120.  2006. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc. Natl. Acad. Sci. USA 103:4962–67 [Google Scholar]
  121. Serra Bonvehí J, Soliva Torrentó M, Centelles Lorente E. 121.  2001. Evaluation of polyphenolic and flavonoid compounds in honeybee-collected pollen produced in Spain. J. Agric. Food Chem. 49:41848–53 [Google Scholar]
  122. Singaravelan N, Inbar M, Ne'eman G, Distl M, Wink M, Izhaki I. 122.  2006. The effects of nectar-nicotine on colony fitness of caged honeybees. J. Chem. Ecol. 32:149–59 [Google Scholar]
  123. Singaravelan N, Nee'man G, Inbar M, Izhaki I. 123.  2005. Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars. J. Chem. Ecol. 31:122791–804 [Google Scholar]
  124. Smirle MJ, Winston ML. 124.  1987. Intercolony variation in pesticide detoxification by the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 80:15–8 [Google Scholar]
  125. Song C, Scharf ME. 125.  2008. Formic acid: a neurologically active, hydrolyzed metabolite of insecticidal formate esters. Pestic. Biochem. Physiol. 92:277–82 [Google Scholar]
  126. Stoner KA, Eitzer BD. 126.  2013. Using a hazard quotient to evaluate pesticide residues detected in pollen trapped from honey bees (Apis mellifera) in Connecticut. PLOS ONE 8:10e77550 [Google Scholar]
  127. Suchail S, De Sousa G, Rahmani R, Belzunces LP. 127.  2004. In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L. Pest Manag. Sci. 60:111056–62 [Google Scholar]
  128. Suchail S, Guez D, Belzunces LP. 128.  2001. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ. Toxicol. Chem. 20:112482–86 [Google Scholar]
  129. Suzuki T, Nojiri H, Isono H, Ochi T. 129.  2004. Oxidative damages in isolated rat hepatocytes treated with the organochlorine fungicides captan, dichlofluanid and chlorothalonil. Toxicology 204:2–397–107 [Google Scholar]
  130. Tahori AS, Sobel Z, Soller M. 130.  1969. Variability in insecticide tolerance of eighteen honey-bee colonies. Entomol. Exp. Appl. 12:185–98 [Google Scholar]
  131. Tapparo A, Giorio C, Marzaro M, Marton D, Soldà L, Girolami V. 131.  2011. Rapid analysis of neonicotinoid insecticides in guttation drops of corn seedlings obtained from coated seeds. J. Environ. Monit. 13:61564–68 [Google Scholar]
  132. Tasei J-N. 132.  2001. Effects of insect growth regulators on honey bees and non-Apis bees: a review. Apidologie 32:6527–45 [Google Scholar]
  133. Thompson HM, Wilkins S, Battersby AH, Waite RJ, Wilkinson D. 133.  2005. The effects of four insect growth-regulating (IGR) insecticides on honeybee (Apis mellifera L.) colony development, queen rearing and drone sperm production. Ecotoxicology 14:7757–69 [Google Scholar]
  134. Tian B, Fadhil NH, Powell JE, Kwong WK, Moran NA. 134.  2012. Long-term exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees. mBio 3:6e00377–12 [Google Scholar]
  135. Tolba MF, Azab SS, Khalifa AE, Abdel-Rahman SZ, Abdel-Naim AB. 135.  2013. Caffeic acid phenethyl ester, a promising component of propolis with a plethora of biological activities: a review on its anti-inflammatory, neuroprotective, hepatoprotective, and cardioprotective effects. IUBMB Life 65:8699–709 [Google Scholar]
  136. Tomás-Barberán FA, Martos I, Ferreres F, Radovic BS, Anklam E. 136.  2001. HPLC flavonoid profiles as markers for the botanical origin of European unifloral honeys. J. Sci. Food Agric. 81:5485–96 [Google Scholar]
  137. Tomizawa M, Casida JE. 137.  2005. Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu. Rev. Pharmacol. Toxicol. 45:247–68 [Google Scholar]
  138. Tomizawa M, Otsuka H, Miyamoto T, Eldefrawi ME, Yamamoto I. 138.  1995. Pharmacological characteristics of insect nicotinic acetylcholine receptor with its ion channel and the comparison of the effect of nicotinoids and neonicotinoids. J. Pestic. Sci. 20:157–64 [Google Scholar]
  139. Tong F, Coats JR. 139.  2012. Quantitative structure–activity relationships of monoterpenoid binding activities to the housefly GABA receptor. Pest Manag. Sci. 68:81122–29 [Google Scholar]
  140. Treutter D. 140.  2005. Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol. 7:6581–91 [Google Scholar]
  141. Umpiérrez ML, Santos E, González A, Rossini C. 141.  2011. Plant essential oils as potential control agents of varroatosis. Phytochem. Rev. 10:2227–44 [Google Scholar]
  142. Underwood RM, Currie RW. 142.  2003. The effects of temperature and dose of formic acid on treatment efficacy against Varroa destructor (Acari: Varroidae), a parasite of Apis mellifera (Hymenoptera: Apidae). Exp. Appl. Acarol. 29:3–4303–13 [Google Scholar]
  143. van den Heever JP, Thompson TS, Curtis JM, Ibrahim A, Pernal SF. 143.  2014. Fumagillin: an overview of recent scientific advances and their significance for apiculture. J. Agric. Food Chem. 62:132728–37 [Google Scholar]
  144. van der Steen JJM, de Kraker J, Grotenhuis T. 144.  2012. Spatial and temporal variation of metal concentrations in adult honeybees (Apis mellifera L.). Environ. Monit. Assess. 184:74119–26 [Google Scholar]
  145. Vidau C, Diogon M, Aufauvre J, Fontbonne R, Viguès B. 145.  et al. 2011. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLOS ONE 6:6e21550 [Google Scholar]
  146. Wahl O, Ulm K. 146.  1983. Influence of pollen feeding and physiological condition on pesticide sensitivity of the honey bee Apis mellifera carnica. Oecologia 59:1106–28 [Google Scholar]
  147. Walz B, Baumann O, Zimmermann B, Ciriacy-Wantrup EV. 147.  1995. Caffeine-sensitive and ryanodine-sensitive Ca2+-induced Ca2+ release from the endoplasmic reticulum in honeybee photoreceptors. J. Gen. Physiol. 105:4537–67 [Google Scholar]
  148. Wiermann R. 148.  1968. Phenylpropanoid metabolism by pollen. I. Survey of flavonoid components isolated from gymnosperms and angiosperms. Ber. Dtsch. Bot. Ges. 81:3–16 [Google Scholar]
  149. Williamson SM, Moffat C, Gomersall MAE, Saranzewa N, Connolly CN, Wright GA. 149.  2013. Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees. Front. Physiol. 4:13 [Google Scholar]
  150. Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA. 150.  et al. 2013. Caffeine in floral nectar enhances a pollinator's memory of reward. Science 339:61241202–4 [Google Scholar]
  151. Wu JY, Anelli CM, Sheppard WS. 151.  2011. Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLOS ONE 6:2e14720Effects of multiple pesticides in wax on larval development. [Google Scholar]
  152. Yu SJ. 152.  2008. The Toxicology and Biochemistry of Insecticides Boca Raton, FL: CRC, 1st ed.. [Google Scholar]
  153. Yu SJ, Robinson FA, Nation JL. 153.  1984. Detoxication capacity in the honey bee, Apis mellifera L. Pestic. Biochem. Physiol. 22:3360–68Detoxification enzyme activity is present in honey bees. [Google Scholar]
  154. Zhu W, Schmehl DR, Mullin CA, Frazier JL. 154.  2014. Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLOS ONE 9:1e77547 [Google Scholar]
  155. Simone-Finstrom MD, Spivak M. 155.  2012. Increased resin collection after parasite challenge: a case of self-medication in honey bees?. PLOS ONE 7:3e34601 [Google Scholar]

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