Evaluation of the distribution and impacts of parasites, pathogens, and pesticides on honey bee (apis mellifera) populations in east Africa

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Muli, Elliud ^a,b   Patch, Harland ^c   Frazier, Maryann ^c   Frazier, James ^c   Torto, Baldwyn ^a   Baumgarten, Tracey ^c   Kilonzo, Joseph ^a   Kimani, James Ng'ang'a ^a   Mumoki, Fiona ^a   Masiga, Daniel ^a   Tumlinson, James ^c   Grozinger, Christina ^c  

^a INTERNATIONAL CENTRE OF INSECT PHYSIOLOGY AND ECOLOGY ICIPE   (Kenya)

^b SOUTH EASTERN KENYA UNIVERSITY   (Kenya)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PESTICIDE;

AFRICA; ANIMAL BEHAVIOR; ARTICLE; ENVIRONMENTAL IMPACT ASSESSMENT; HONEYBEE; HOST PARASITE INTERACTION; HYGIENE; KENYA; NONHUMAN; NOSEMA; ORGANISM COLONY; PARASITE CONTROL; PARASITE IDENTIFICATION; PARASITE LOCALIZATION; PARASITE MIGRATION; POPULATION ABUNDANCE; SURVIVAL RATE; VARROA; VARROOSIS; VIRUS IDENTIFICATION; ANIMAL; BEE; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL PROTECTION; HOST PATHOGEN INTERACTION; PARASITOLOGY; PHYSIOLOGY; POLLINATION; POPULATION DYNAMICS; TOXICITY; VARROIDAE;

AFRICA, EASTERN; ANIMALS; BEES; CONSERVATION OF NATURAL RESOURCES; ENVIRONMENTAL EXPOSURE; HOST-PATHOGEN INTERACTIONS; PESTICIDES; POLLINATION; POPULATION DYNAMICS; VARROIDAE;

EID: 84899713807     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094459     Document Type: Article

References (77)

1. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, et al. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B-Biological Sciences 274: 303-313. (Pubitemid 47055453)
2. Eilers EJ, Kremen C, Greenleaf SS, Garber AK, Klein AM (2011) Contribution of Pollinator-Mediated Crops to Nutrients in the Human Food Supply. Plos One 6.
3. Gallai N, Salles JM, Settele J, Vaissiere BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68: 810-821.
4. Klein AM, Steffan-Dewenter I, Tscharntke T (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proceedings of the Royal Society of London Series B-Biological Sciences 270: 955-961. (Pubitemid 36561032)
5. Bhattacharya A (2004) Flower visitor and fruitset of Anacardium occidentole. Annales Botanici Fennici 41: 385-392. (Pubitemid 40113067)
6. Roubik DW (2002) The value of bees to the coffee harvest. Nature 417: 708.
7. Aizen MA, Harder LD (2009) The Global Stock of Domesticated Honey Bees Is Growing Slower Than Agricultural Demand for Pollination. Current Biology 19: 915-918.
8. Morse RA, Calderone NW (2000) The value of honey bees as pollinators of U.S. crops in 2000. Bee Culture 128: 1-15.
9. Allsopp M (2004) Cape honeybee (Apis mellifera capensis Eshscholtz) and varroa mite (Varroa destructor Anderson & Trueman) threats to honeybees and beekeeping in Africa. International Journal of Tropical Insect Science 24: 87-94. (Pubitemid 43211516)
10. 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. Journal of Invertebrate Pathology 103: S80-S95.
11. Sammataro D, Gerson U, Needham G (2000) Parasitic mites of honey bees: life history, implications, and impact. Annu Rev Entomol 45: 519-548. (Pubitemid 30187872)
12. Chen YP, Huang ZY (2010) Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie 41: 364-374.
13. Chen YP, Siede R (2007) Honey Bee Viruses. In: Maramorosh K, Shatkin AJ, Murphy FA, editors. Advances in Virus Research: Elsevier Academic Press. pp. 34-80.
14. Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D, et al. (2011) Temporal Analysis of the Honey Bee Microbiome Reveals Four Novel Viruses and Seasonal Prevalence of Known Viruses, Nosema, and Crithidia. Plos One 6.
15. Aronstein KA, Murray KD (2010) Chalkbrood disease in honey bees. J Invertebr Pathol 103 Suppl 1: S20-S29.
16. Genersch E (2008) Paenibacillus larvae and American Foulbrood - long since known and still surprising. Journal fur Verbrauchershutz und Lebensmittelsicherheit 3: 429-434.
17. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52: 81-106. (Pubitemid 46133563)
18. Brodschneider R, Crailsheim K (2010) Nutrition and health in honey bees. Apidologie 41: 278-294.
19. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317: 362-364. (Pubitemid 47106374)
20. VanEngelsdorp D, Caron D, Hayes J, Underwood R, Henson M, et al. (2012) A national survey of managed honey bee 2010-11 winter colony losses in the USA: results from the Bee Informed Partnership. Journal of Apicultural Research 51: 115-124.
21. Chauzat MP, Carpentier P, Madec F, Bougeard S, Cougoule N, et al. (2010) The role of infectious agents and parasites in the health of honey bee colonies in France. Journal of Apicultural Research 49: 31-39.
22. 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. (Pubitemid 47574857)
23. Nguyen BK, Ribiere M, vanEngelsdorp D, Snoeck C, Saegerman C, et al. (2011) Effects of honey bee virus prevalence, Varroa destructor load and queen condition on honey bee colony survival over the winter in Belgium. Journal of Apicultural Research 50: 195-202.
24. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, et al. (2009) Colony collapse disorder: A descriptive study. Plos One 4: e6481.
25. vanEngelsdorp D, Speybroeck N, Evans JD, Nguyen BK, Mullin C, et al. (2010) Weighing risk factors associated with bee colony collapse disorder by classification and regression tree analysis. J Econ Entomol 103: 1517-1523.
26. Hepburn RH, Radloff SE (1998) Honeybees of Africa. New York: Springer. 386 p.
27. Ruttner F (1987) Biogeography and Taxonomy of Honeybees: Springer. 284 p.
28. Meixner MD, Leta MA, Koeniger N, Fuchs S (2011) The honey bees of Ethiopia represent a new subspecies of Apis mellifera-Apis mellifera simensis n. ssp. Apidologie 42: 425-437.
29. Whitfield CW, Behura SK, Berlocher SH, Clark AG, Johnston JS, et al. (2006) Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science 314: 642-645. (Pubitemid 44646386)
30. Crane E (1999) The World History of Bee Keeping and Honey Hunting New York: Routledge. 720 p.
31. Mbae RM (1999) Overview of beekeeping development in Kenya. In: Raina SK, Kioka EN, Mwanycky SW, editors. The Conservation and Utilization of Commercial Insects. Nairobi: ICIPE Science Press. pp. 103-105.
32. Kasina M, Kraemer M, Martius C, Wittmann D (2009) Diversity and Activity Density of Bees Visiting Crop Flowers in Kakamega, Western Kenya. Journal of Apicultural Research 48: 134-139.
33. UNCTAD/WTO ITC (2004) Kenya: Supply Suvery on Apicultural and Horticultural Products. Geneva, Switzerland: International Trade Centre.
34. National Beekeeping Station (2007) Hive Population and Production in Kenya (2005, 2006, and 2007) Provincial Summaries. Nairobi, Kenya: Ministry of Livestock.
35. Frazier M, Muli E, Conklin T, Schmehl D, Torto B, et al. (2010) A scientific note on Varroa destructor found in East Africa; threat or opportunity? Apidologie 41: 463-465.
36. Wei S (2001) Genetic Variation and Colony Development of Honey Bees Apis mellifera in Kenya. Uppsala: Swedish University of Agricultrual Sciences. 22 p.
37. DiPrisco G, Pennacchio F, Caprio E, Boncristiani HF Jr., Evans JD, et al. (2011) Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J Gen Virol 92: 151-155.
38. Gisder S, Aumeier P, Genersch E (2009) Deformed wing virus: replication and viral load in mites (Varroa destructor). J Gen Virol 90: 463-467.
39. Ellis MD, Macedo PA (2001) G01-1430 Using the Sugar Roll Technique to Detect Varroa Mites in Honey Bee Colonies. Lincoln, NE: University of Nebraska. 4 p.
40. Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, et al. (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96: 1-10. (Pubitemid 47260581)
41. Fries I, Chauzat MP, Chen YP, Doublet V, Genersch E, Gisder S, Higes M, McMahon DP, Martin-Hernandez R, Natsopoulou M, Paxton RJ, Tanner G, Webster TC, Williams GR (2013) Standard methods for Nosema research. Journal of Apicultural Research 51(5): http://dx.doi.org/10.3896/IBRA.1.52.1.14.
42. Traver BE, Fell RD (2011) "Prevalence and infection intensity of Nosema in honey bee (Apis mellifera L.) colonies in Virginia." Journal of Invertebrate Pathology 107(1): 43-49.
43. Benjeddou M, Leat N, Allsopp M, Davison S (2001) Detection of acute bee paralysis virus and black queen cell virus from honeybees by reverse transcriptase pcr. Appl Environ Microbiol 67: 2384-2387. (Pubitemid 33641434)
44. Chen YP, Higgins JA, Feldlaufer MF (2005) Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Appl Environ Microbiol 71: 436-441. (Pubitemid 40116299)
45. Ribiere M, Triboulot C, Mathieu L, Aurieres C, Faucon JP, et al. (2002) Molecular diagnosis of chronic bee paralysis virus infection. Apidologie 33: 339- 351. (Pubitemid 34600978)
46. Stoltz D, Shen XR, Boggis C, Sisson G (1995) Molecular diagnosis of Kashmir bee virus infection. Journal of Apicultural Research 34: 153-160. (Pubitemid 126003831)
47. Spivak M, Reuter GS (1998) Honey bee hygienic behavior. American Bee Journal 138: 283-286.
48. Arias MC, Sheppard WS (1996) Molecular phylogenetics of honey bee subspecies (Apis mellifera L.) inferred from mitochondrial DNA sequence. Mol Phylogenet Evol 5: 557-566. (Pubitemid 126320901)
49. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680. (Pubitemid 24354800)
50. Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
51. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, et al. (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. Plos One 5: e9754.
52. Delaplane KS, Hood WM (1997) Effects of delayed acaricide treatment in honey bee colonies parasitized by Varroa jacobsoni and a late season treatment threshold for the southeastern USA. Journal of Apicultural Research 36: 125- 132.
53. Ruttner F (1992) Naturgeschichte der Honigbienen: Kosmos Verlags-GmbH.
54. Spivak M, Reuter GS (2001) Varroa destructor infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. Journal of Economic Entomology 94: 326-331. (Pubitemid 33749917)
55. Akinwade KL, Badejo MA, Ogbogu SS (2012) Incidence of the Korea haplotype of Varroa destructor in southwest Nigeria. Journal of Apicultural Research 15: 369- 370.
56. Guzman-Novoa E, Vandame Rm, Arechavaleta M E. (1999) Susceptibility of European and Africanized honey bees (Apis mellifera L.) to Varroa jacobsoni Oud. in Mexico. Apidologie 30: 173-182. (Pubitemid 29260682)
57. Fries I, Hansenb H, Imdorfc A, Rosenkranz P (2003) Swarming In Honey Bees (Apis Mellifera) And Varroa Destructor Population Development In Sweden Apidologie 34: 389-397.
58. National Bee Unit (2010) FAQ 17: Queen trapping. York: The Food and Environmental Research Agency. 1-2 p.
59. Calderone NW (2005) Evaluation of drone brood removal for management of Varroa destructor (Acari: Varroidae) in colonies of Apis mellifera (Hymenoptera: Apidae) in the northeastern United States. J Econ Entomol 98: 645-650. (Pubitemid 40841439)
60. Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE, et al. (2012) Global honey bee viral landscape altered by a parasitic mite. Science 336: 1304- 1306.
61. Kajobe R, Marris G, Budge G, Laurenson L, Cordoni G, et al. (2010) First molecular detection of a viral pathogen in Ugandan honey bees. J Invertebr Pathol 104: 153-156.
62. Pirk CWW, deMiranda JR, Kramer M, Murray TE, Nazzi F, et al (2013) "Statistical guidelines for Apis mellifera research." Journal of Apicultural Research 52(4).
63. Highfield AC, El Nagar A, Mackinder LC, Noel LM, Hall MJ, et al. (2009) Deformed wing virus implicated in overwintering honeybee colony losses. Appl Environ Microbiol 75: 7212-7220.
64. Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P (2012) Predictive markers of honey bee colony collapse. Plos One 7: e32151.
65. Schoning C, Gisder S, Geiselhardt S, Kretschmann I, Bienefeld K, et al. (2012) Evidence for damage-dependent hygienic behaviour towards Varroa destructorparasitised brood in the western honey bee, Apis mellifera. J Exp Biol 215: 264- 271.
66. Higes M, Martin-Hernandez R, Botias C, Bailon EG, Gonzalez-Porto AV, et al. (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10: 2659-2669.
67. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, et al. (2012) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci U S A 108: 662-667.
68. Pettis JS, vanEngelsdorp D, Johnson J, Dively G (2012) Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99: 153-158.
69. Fries I, Slamenda SB, Da Silva A, Pieniazek NJ (2003) African honey bees (Apis mellifera scutellata) and Nosema (Nosema apis) infections. Journal of Apicultural Research 42: 13-15. (Pubitemid 36755345)
70. Swart DJ (2003) The occurence of Nosema apis (Zander), Acarapis woodi (Rennie), and the Cape problem bee in the summer rainfall region of South Africa Rhodes University. 43 p.
71. Faucon J-P, Mathieu L, Ribiere M, Martel A-C, Drajnudel P, et al. (2002) Honey bee winter mortality in France in 1999 and 2000. Bee World 83 14-23. (Pubitemid 34978830)
72. Zhu W, Schmehl DR, Mullin CA, Frazier JL (submitted) Chronic oral toxicity of four commone pesticides and their mixtures to honey bee larvae.
73. Bortolotti L, Montanari R, Marcelino J, Medrzycki P, Maini S, et al. (2003) Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bulletin of Insectology 56: 63-67.
74. Ciarlo TJ, Mullin CA, Frazier JL, Schmehl DR (2012) Learning impairment in honey bees caused by agricultural spray adjuvants. Plos One 7: e40848.
75. Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delegue MH (2004) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57: 410-419. (Pubitemid 38376274)
76. 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.
77. Wu JY, Smart MD, Anelli CM, Sheppard WS (2012) Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. J Invertebr Pathol 109: 326-329.