High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee Health

PLoS ONE

Volumn 5, Issue 3, 2010, Pages

  Mullin, Christopher A ^a   Frazier, Maryann ^a   Frazier, James L ^a   Ashcraft, Sara ^a   Simonds, Roger ^b   vanEngelsdorp, Dennis ^c   Pettis, Jeffery S ^d  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

^c Pennsylvania Department of Agriculture   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACARICIDE; AGRICULTURAL CHEMICAL; CHLOROTHALONIL; HERBICIDE; NITRILE; PESTICIDE;

ANIMAL; APICULTURE; ARTICLE; BEE; DRUG EFFECT; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METHODOLOGY; NORTH AMERICA; POLLEN; TIME;

ACARICIDES; AGROCHEMICALS; ANIMALS; BEEKEEPING; BEES; CHROMATOGRAPHY, LIQUID; HERBICIDES; MASS SPECTROMETRY; NITRILES; NORTH AMERICA; PESTICIDES; POLLEN; TIME FACTORS;

EID: 79952118619     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009754     Document Type: Article

References (76)

1. vanEngelsdorp D, Underwood R, Caron D, Hayes J (2007) An estimate of managed colony losses in the winter of 2006-2007: A report commissioned by the Apiary Inspectors of America. Am Bee J 147: 599-603.
2. vanEngelsdorp D, Hayes J, Jr., Underwood RM, Pettis J (2008) A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS ONE 3: 1-6 e4071.
3. vanEngelsdorp D, Hayes J, Jr., Underwood RM, Pettis JS (2010) A survey of honey bee colony losses in the United States, fall 2008 to spring 2009. J Apic Res 49: 7-14.
4. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313: 351-354.
5. Faucon JP, Mathieu L, Ribiere M, Martel AC, Drajnudel P, et al. (2002) Honey bee winter mortality in France in 1999 and 2000. Bee World 83: 14-23.
6. Finley J, Camazine S, Frazier M (1996) The epidemic of honey bee colony losses during the 1995-1996 season. Am Bee J 136: 805-808.
7. Bonmatin JM, Marchand PA, Charvet R, Moineau I, Bengsch ER, et al. (2005) Quantification of imidacloprid uptake in maize crops. J Agric Food Chem 53: 5336-5341.
8. Chauzat MP, Faucon JP, Martel AC, Lachaize J, Cougoule N, et al. (2006) A survey of pesticide residues in pollen loads collected by honey bees in France. J Econ Entomol 99: 253-262.
9. Halm MP, Rortais A, Arnold G, Tasei JN, Rault S (2006) New risk assessment approach for systemic insecticides: The case of honey bees and imidacloprid (Gaucho). Environ Sci Technol 40: 2448-2454.
10. Decourtye A, Armengaud C, Renou M, Devillers J, Cluzeau S, et al. (2004) Imidacloprid impairs memory and brain metalbolism in the honeybee (Apis mellifera L.). Pestic Biochem Physiol 78: 83-92.
11. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial Arthropods. Annu Rev Entomol 52: 81-106.
12. Alder L, Greulich K, Kempe G, Vieth B (2006) Residue analysis of 500 high priority pesticides: Better by GC-MS or LC-MS/MS? Mass Spectrom Rev 25: 838-865.
13. Ferrer I, Thurman EM (2007) Multi-residue method for the analysis of 101 pesticides and their 14 degradates in food and water samples by liquid chromatography/time-of-flight mass spectrometry. J Chromatogr A 1175: 24-37.
14. Rortais A, Arnold G, Halm MP, Touffet-Briens F (2005) Modes of honeybees exposure to systemic insecticides: Estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36: 71-83.
15. Kindemba V (2009) The impact of neonicotinoid insecticides on bumblebees, honey bees and other non-target invertebrates. Buglife. Available: http://www. buglife.org.uk/News/Pesticides+Poisoning+Our+Bees.htm.
16. Frazier M, Mullin C, Frazier J, Ashcraft S (2008) What have pesticides got to do with it? Am Bee J 148: 521-523.
17. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, et al. (2007) A metagenomic survey of microbes in honey bee Colony Collapse Disorder. Science 318: 283-287.
18. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, et al. (2009) Colony Collapse Disorder: A descriptive study. PLoS ONE 4: 1-17 e6481.
19. Tierney KB, Sampson JL, Ross PS, Sekela MA, Kennedy CJ (2008) Salmon olfaction is impaired by an environmentally realistic pesticide mixture. Environ Sci Technol 42: 4996-5001.
20. Fox JE, Gulledge J, Engelhaupt E, Burow ME, McLachlan JA (2007) Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proc Natl Acad Sci USA 104: 10282-10287.
21. Hayes TB, Case P, Chui S, Chung D, Haeffele C, et al. (2006) Pesticide mixtures, endocrine disruption, and amphibian declines: Are we underestimating the impact? Environ Health Perspect 114: 40-50.
22. Rohr JR, Raffel TR, Sessions SK, Hudson PJ (2008) Understanding the net effects of pesticides on amphibian trematode infections. Ecol Appl 18: 1743-1753.
23. Bat Conservation International (2009) What we do/ white-nose syndrome. Available: http://www.batcon.org/index.php/what-we-do/white-nose-syndrome. html. Accessed 2009 Oct 7.
24. vanEngelsdorp D, Evans JD, Donovall L, Mullin C, Frazier M, et al. (2009) ''Entombed pollen'': A new condition in honey bee colonies associated with increased risk of colony mortality. J Invert Pathol 101: 147-149.
25. Lehotay SJ, Mastovska K, Lightfield AR (2005) Use of buffering and other means to improve results of problematic pesticides in a fast and easy method for residue analysis of fruits and vegetables. J AOAC Int 88: 615-629.
26. BfR (2009) Parameters for the determination of pesticide residues. Available: http://www.bfr.bund.de/cd/5832.
27. Atkins EL, Kellum D, Atkins KW (1981) Reducing pesticide hazards to honey bees: Mortality prediction and integrated management strategies. Univ Calif Div Agric Sci Leafl 2883.
28. Atkins EL, Kellum D (1986) Comparative morphogenic and toxicity studies on the effect of pesticides on honeybee brood. J Apic Res 25: 242-255.
29. Graham JM, editor (1992) The hive and the honey bee. Hamilton, IL: Dadant & Sons. pp 1324 p.
30. Aldridge WN, Reiner E (1969) Acetylcholinesterase-Two types of inhibition by an organophosphorus compound: One the formation of phosphorylated enzyme and the other analogous to inhibition by substrate. Biochem J 115: 147-162.
31. Wheelock CE (1959) The fluorescence of some coumarins. J Am Chem Soc 81: 1348-1352.
32. Chauzat MP, Carpentier P, Martel AC, Bougeard S, Cougoule N, et al. (2009) Influence of pesticide residues on honey bee (Hymenoptera: Apidae) colony health in France. Environ Entomol 38: 514-523.
33. Crailsheim K, Schneider LHW, Hrassnigg N, Buhlmann G, Brosch U, et al. (1992) Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): Dependence on individual age and function. J Insect Physiol. 38: 409-419.
34. Jones AK, Raymond-Delpech V, Thany SH, Gauthier M, Sattelle DB (2006) The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. Genome Res 16: 1422-1430.
35. Everich R, Schiller C, Whitehead J, Beavers M, Barrett K (2009) Effects of captan on Apis mellifera brood development under field conditions in California almond orchards. J Econ Entomol 102: 20-29.
36. Kubik M, Nowacki J, Pidek A, Warakomska Z, Michalczuk L, et al. (1999) Pesticide residues in bee products collected from cherry trees protected during blooming period with contact and systemic fungicides. Apidologie 30: 521-532.
37. Chaves A, Shea D, Danehower D (2008) Analysis of chlorothalonil and degradation products in soil and water by GC/MS and LC/MS. Chemosphere 71: 629-638.
38. Munn MD, Gilliom RJ (2001) Pesticide toxicity index for freshwater aquatic organisms. U.S. Geological Survey Water-Resources Investigations Report 01-4077. Sacramento, CA.
39. Ladurner E, Bosch J, Kemp WP, Maini S (2005) Assessing delayed and acute toxicity of five formulated fungicides to Osmia lignaria Say and Apis mellifera. Apidologie 36: 449-460.
40. Bogdanov S, Kilchenmann V, Imdorf A (1998) Acaricide residues in some bee products. J Apic Res 37: 57-67.
41. Lodesani M, Pellacani A, Bergomi S, Carpana E, Rabitti T, et al. (1992) Residue determination for some products used against Varroa infestation in bees. Apidologie 23: 257-272.
42. Wallner K (1995) The use of varroacides and their influence on the quality of bee products. Am Bee J 135: 817-821.
43. Bogdanov S (2004) Beeswax: quality issues today. Bee World 85: 46-50.
44. Tremolada P, Bernardinelli I, Colombo M, Spreafico M, Vighi M (2004) Coumaphos distribution in the hive ecosystem: Case study for modeling applications. Ecotoxicology 13: 589-601.
45. Martel AC, Zeggane S, Aurieres C, Drajnudel P, Faucon JP, et al. (2007) Acaricide residues in honey and wax after treatment of honey bee colonies with ApivarH or AsuntolH50. Apidologie 38: 534-544.
46. Collins AM, Pettis JS, Wilbanks R, Feldlaufer MF (2004) Performance of honey bee (Apis mellifera) queens reared in beeswax cells impregnated with coumaphos. J Apic Res 43: 128-134.
47. Lodesani M, Costa M (2005) Limits of chemotherapy in beekeeping: Development of resistance and the problem of residues. Bee World 86: 102-109.
48. Johnson RM, Pollock HS, Berenbaum MR (2009) Synergistic interactions between in-hive miticides in Apis mellifera. J Econ Entomol 102: 474-479.
49. Pilling ED, Jepson PC (1993) Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera). Pestic Sci 39: 293-297.
50. Mineau P, Harding KM, Whiteside M, Fletcher MR, Garthwaite D, et al. (2008) Using reports of bee mortality in the field to calibrate laboratory-derived pesticide risk indices. Environ Entomol 37: 546-554.
51. vanDame R, Meled M, Colin ME, Belzunces LP (1995) Alteration of the homing-flight in the honey bee Apis mellifera L. exposed to sublethal dose of deltamethrin. Environ Toxicol Chem 14: 855-860.
52. Thompson H, Wilkins S (2003) Assessment of the synergy and repellency of pyrethroid/fungicide mixtures. Bulletin of Insectology 56: 131-134.
53. Ellis MD, Siegfried BD, Spawn B (1997) The effect of ApistanH on honey bee (Apis mellifera L): Responses to methyl parathion, carbaryl and bifenthrin exposure. Apidologie 28: 123-127.
54. Cox RL, Wilson WT (1984) Effects of permethrin on the behavior of individually tagged honey bees, Apis mellifera L (Hymenoptera, Apidae). Environ Entomol 13: 375-378.
55. Anderson JF, Wojtas MA (1986) Honey bees (Hymenoptera, Apidae) contaminated with pesticides and polychlorinated biphenyls. J Econ Entomol 79: 1200-1205.
56. Walorczyk S, Gnusowski B (2009) Development and validation of a multiresidue method for the determination of pesticides in honeybees using acetonitrile-based extraction and gas chromatography-tandem quadrupole mass spectrometry. J. Chromatogr. A 1216: 6522-6531.
57. Ghini S, Fernandez M, Pico Y, Marin R, Fini F, et al. (2004) Occurrence and distribution of pesticides in the province of Bologna, Italy, using honeybees as bioindicators. Arch Environ ContamToxicol 47: 479-488.
58. Johansen CA, Rincker CM, George DA, Mayer DF, Kious CW (1984) Effects of aldicarb and its biologically-active metabolites on bees. Environ. Entomol. 13: 1386-1398.
59. Thompson HM (2003) Behavioral effects of pesticides in bees-their potential for use in risk assessment. Ecotoxicology 12: 317-330.
60. Wahl O, Ulm K (1983) Influence of pollen feeding and physiological condition on pesticide sensitivity of the honey bee Apis mellifera carnica. Oecologia 59: 106-128.
61. Gilliam M (1997) Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol Lett 155: 1-10.
62. DeGrandi-Hoffman G, Sammataro D, Alarcon R (2009) The importance of microbes in nutrition and health of honey bee colonies. Part 1. Am Bee J 149: 583-584.
63. Maude RB (1996) Disease control: Eradication and reduction of inoculum by seed treatment. In: Maude RB, ed. Seedborne diseases and their control: Principles and practice, Wallingford, UK: CAB International. pp 114-178.
64. Halmer P (2000) Commercial seed treatment technology. In: Black M, Bewley JD, eds. Seed technology and its biological basis. Sheffield, UK: CRC Sheffield Academic Press. pp 257-286.
65. Mullin CA, Saunders MC, Leslie TW, Biddinger DJ, Fleischer SJ (2005) Toxic and behavioral effects to Carabidae of seed treatments used on Cry3Bbl-and Cry1Ab/c-protected corn. Environ Entomol 34: 1626-1636.
66. Iwasa T, Motoyama N, Ambrose JT, Roe RM (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot 23: 371-378.
67. Everts S (2008) Honeybee loss-Agriculture: Germany suspends use of clothianidin after the pesticide is linked to honeybee deaths. Chem Eng News 86(21): 10.
68. Nguyen BK, Saegerman C, Pirard C, Mignon J, Widart J, et al. (2009) Does imidacloprid seed-treated maize have an impact on honey bee mortality? J Econ Entomol 102: 616-623.
69. Schmuck R, Stadler T, Schmidt HW (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 Mgt Sci 59: 279-286.
70. EPA-OPP (2005) Reregistration eligibility decision for tau-fluvalinate. Docket. pp 2005-0230.
71. Johnson RM, Wen ZM, Schuler MA, Berenbaum MR (2006) Mediation of pyrethroid insecticide toxicity to honey bees (Hymenoptera: Apidae) by cytochrome P450 monooxygenases. J Econ Entomol 99: 1046-1050.
72. Martin SJ (2004) Acarcide (pyrethroid) resistance in Varroa destructor. Bee World 85: 67-69.
73. Pettis JS, Shimanuki H, Feldlaufer MF (1998) An assay to detect fluvalinate resistance in Varroa mites. Am Bee J 138: 538-541.
74. Sammataro D, Untalan P, Guerrero F, Finley J (2005) The resistance of varroa mites (Acari: Varroidae) to acaricides and the presence of esterase. Int J Acarol 31: 67-74.
75. Elzen PJ, Baxter JR, Spivak M, Wilson WT (2000) Control of Varroa jacobsoni Oud. resistant to fluvalinate and amitraz using coumaphos. Apidologie 31: 437-441.
76. USDA-AMS (2008) Pesticide data program: Annual summary, calendar year 2007 Available: http://www.ams.usda.gov/pdp.