Honey bee colony losses and associated viruses

Current Opinion in Insect Science

Volumn 8, Issue , 2015, Pages 121-129

  McMenamin, Alexander J ^a   Genersch, Elke ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Institute for Bee Research   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84939992946     PISSN: 22145745     EISSN: 22145753     Source Type: Journal    
DOI: 10.1016/j.cois.2015.01.015     Document Type: Review

References (87)

1. G. Bloch, T.M. Francoy, I. Wachtel, N. Panitz-Cohen, S. Fuchs, and A. Mazar Industrial apiculture in the Jordan valley during Biblical times with Anatolian honeybees Proc Natl Acad Sci USA 107 2010 11240 11244
2. L.A. Garibaldi, I. Steffan-Dewenter, R. Winfree, M.A. Aizen, R. Bommarco, S.A. Cunningham, C. Kremen, L.G. Carvalheiro, L.D. Harder, and O. Afik et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance Science 339 2013 1608 1611
3. R.A. Morse, and N.W. Calderone The value of honey bee pollination in the United States Bee Culture 128 2000 1 15
4. M.A. Aizen, L.A. Garibaldi1, S.A. Cunningham, and A.M. Klein How much does agriculture depend on pollinators? Lessons from long-term trends in crop production Ann Bot (Lond) 103 2009 1579 1588
5. M.H. Allsopp, W.J. de Lange, and R. Veldtman Valuing insect pollination services with cost of replacement PLoS ONE 3 2008 e3128
6. M.A. Aizen, and L.D. Harder The global stock of domesticated honey bees is growing slower than agricultural demand for pollination Curr Biol 19 2009 915 918
7. D. vanEngelsdorp, and M.D. Meixner 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 2010 S80 S95
8. N. Gallai, J.-M. Salles, J. Settele, and B.E. Vaissiere Economic valuation of the vulnerability of world agriculture confronted with pollinator decline Ecol Econ 68 2009 810 821
9. E.J. Eilers, C. Kremen, S. Smith Greenleaf, A.K. Garber, and A.M. Klein Contribution of pollinator-mediated crops to nutrients in the human food supply PLoS ONE 6 2011 e21363
10. M. Aizen, L. Garibaldi, S. Cunningham, and A. Klein Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency Curr Biol 18 2008 1572 1575
11. D. Goulson, M.E. Hanley, B. Darvill, and J.S. Ellis Biotope associations and the decline of bumblebees (Bombus spp.) J Insect Conserv 10 2006 95 103
12. L.A. Burkle, J.C. Marlin, and T.M. Knight Plant-pollinator interactions over 120 years: loss of species, co-occurrence and function Science 339 2013 1611 1615
13. S.A. Cameron, J.D. Loziera, J.P. Strange, J.B. Koch, N. Cordes, L.F. Solter, and T.L. Griswold Patterns of widespread decline in North American bumble bees Proc Natl Acad Sci USA 108 2011 662 667
14. R. Dukas Mortality rates of honey bees in the wild Insect Soc 55 2008 252 255
15. E. Genersch Honey bee pathology: current threats to honey bees and beekeeping Appl Microbiol Biotechnol 87 2010 87 97
16. E. Genersch, W. von der Ohe, H. Kaatz, A. Schroeder, C. Otten, R. Büchler, S. Berg, W. Ritter, W. Mühlen, and S. Gisder et al. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies Apidologie 41 2010 332 352
17. D. vanEngelsdorp, J.D. Evans, C. Saegerman, C. Mullin, E. Haubruge, B.K. Nguyen, M. Frazier, J. Frazier, D. Cox-Foster, and Y. Chen et al. Colony collapse disorder: a descriptive study PLoS ONE 4 2009 e6481
18. S.G. Potts, S.P.M. Roberts, R. Dean, G. Marris, M.A. Brown, H.R. Jones, P. Neumann, and J. Settele Declines of managed honey bees and beekeepers in Europe J Apicult Res 49 2010 15 22
19. F.L.W. Ratnieks, and N.L. Carreck Clarity on honey bee collapse? Science 327 2010 152 153
20. G.R. Williams, D.R. Tarpy, D. vanEngelsdorp, M.-P. Chauzat, D.L. Cox-Foster, K.S. Delaplane, P. Neumann, J.S. Pettis, R.E.L. Rogers, and D. Shutler Colony collapse disorder in context Bioessays 32 2010 845 846
21. D. vanEngelsdorp, J. Hayes Jr., R.M. Underwood, and J. Pettis A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008 PLoS ONE 3 2008 e4071
22. D. vanEngelsdorp, J. Hayes Jr., R.M. Underwood, and J.S. Pettis A survey of honey bee colony losses in the United States, fall 2008 to spring 2009 J Apic Res 49 2010 7 14
23. D. vanEngelsdorp, R. Underwood, D. Caron, and J. Hayes 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 2007 599 603
24. Y.-P. Chen, and R. Siede Honey bee viruses Adv Virus Res 70 2007 33 80
25. C. Runckel, M.L. Flenniken, J.C. Engel, J.G. Ruby, D. Ganem, R. Andino, and J.L. DeRisi Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia PLoS ONE 6 2011 e20656
26. J.L. Li, R.S. Cornman, J.D. Evans, J.S. Pettis, Y. Zhao, C. Murphy, W.J. Pen, J. Wu, M. Hamilton, and H.F. Boncristiani et al. Systemic spread and propagation of a plant-pathogenic virus in European honeybees, Apis mellifera mBio 5 2014 e00898-00813
27. R.S. Hails, B.V. Ball, and E. Genersch Infection strategies of insect viruses M. Aubert, B.V. Ball, I. Fries, R.F.A. Moritz, N. Milani, I. Bernardinelli, Virology and the Honey Bee 2008 European Communities 255 275
28. B.V. Ball, and L. Bailey Viruses R.A. Morse, K. Flottum, Honey Bee Pests, Predators and Diseases edn 3rd 1997 Peacock Press 11 31
29. D. Tentcheva, L. Gauthier, N. Zappulla, B. Dainat, F. Cousserans, M.E. Colin, and M. Bergoin Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France Appl Environ Microbiol 70 2004 7185 7191
30. A. Baker, and D. Schroeder Occurrence and genetic analysis of picorna-like viruses infecting worker bees of Apis mellifera L. populations in Devon, South West England J Invertebr Pathol 98 2008 239 242
31. L. Gauthier, D. Tentcheva, M. Tournaire, B. Dainat, F. Cousserans, M.E. Colin, and M. Bergoin Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique Apidologie 38 2007 426 435
32. A.L. Levitt, R. Singh, D.L. Cox-Foster, E. Rajotte, K. Hoover, N. Ostiguy, and E.C. Holmes Cross-species transmission of honey bee viruses in associated arthropods Virus Res 176 2013 232 240
33. R. Singh, A.L. Levitt, E.G. Rajotte, E.C. Holmes, N. Ostiguy, D. vanEngelsdorp, W.I. Lipkin, C.W. dePamphilis, A.L. Toth, and D.L. Cox-Foster RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species PLoS ONE 5 2010 e14357
34. E. Genersch, C. Yue, I. Fries, and J.R. de Miranda Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities J Invertebr Pathol 91 2006 61 63
35. M.A. Fürst, D.P. McMahon, J.L. Osborne, R.J. Paxton, and M.F. Brown Disease associations between honey bees and bumblebees as a threat to the wild pollinators Nature 506 2014 364 366
36. P. Rosenkranz, P. Aumeier, and B. Ziegelmann Biology and control of Varroa destructor J Invertebr Pathol 103 2010 S96 S119
37. J.R. de Miranda, and E. Genersch Deformed wing virus J Invertebr Pathol 103 2010 S48 S61
38. J.R. de Miranda, G. Cordoni, and G. Budge The acute bee paralysis virus - Kashmir bee virus - Israeli acute paralysis virus complex J Invertebr Pathol 103 2010 S30 S47
39. E. Genersch, and M. Aubert Emerging and re-emerging viruses of the honey bee (Apis mellifera) Vet Res 41 2010 54
40. D.L. Cox-Foster, S. Conlan, E.C. Holmes, G. Palacios, J.D. Evans, N.A. Moran, P.-L. Quan, S. Briese, M. Hornig, and D.M. Geiser et al. A metagenomic survey of microbes in honey bee colony collapse disorder Science 318 2007 283 287
41. V. Soroker, A. Hetzroni, B. Yakobson, D. David, A. David, H. Voet, Y. Slabezki, H. Efrat, S. Levski, and Y. Kamer et al. Evaluation of colony losses in Israel in relation to the incidence of pathogens and pests Apidologie 42 2011 192 199
42. N. Bacandritsos, A. Granato, G. Budge, I. Papanastasiou, E. Roinioti, M. Caldon, C. Falcaro, A. Gallina, and F. Mutinelli Sudden seaths and colony population decline in Greek honey bee colonies J Invertebr Pathol 105 2010 335 340
43. M.D. Meixner, R.M. Francis, A. Gajda, P. Kryger, S. Andonov, A. Uzunov, G. Topolska, C. Costa, E. Amiri, and S. Berg et al. Occurrence of parasites and pathogens in honey bee colonies used in a European genotype-environment interactions experiment J Apicult Res 53 2014 215 229
44. O. Berenyi, T. Bakonyi, I. Derakhshifar, H. Köglberger, and N. Nowotny Occurence of six honeybee viruses in diseased Austrian apiaries Appl Environ Microbiol 72 2006 2414 2420
45. S.L. Nielsen, M. Nicolaisen, and P. Kryger Incidence of acute bee paralysis virus, black queen cell virus, chronic bee paralysis virus, deformed wing virus, Kashmir bee virus and sacbrood virus in honey bees (Apis mellifera) in Denmark Apidologie 39 2008 310 314
46. F. Granberg, M. Vicente-Rubiano, C. Rubio-Guerri, O.E. Karlsson, D. Kukielka, S. Belák, and J.M. Sánchez-Vizcaíno Metagenomic detection of viral pathogens in Spanish honeybees: co-infection by Aphid lethal paralysis, Israel acute paralysis and Lake Sinai viruses PLoS ONE 8 2013 e57459
47. R.S. Cornman, D.R. Tarpy, Y. Chen, L. Jeffreys, D. Lopez, J.S. Pettis, D. vanEngelsdorp, and J.D. Evans Pathogen webs in collapsing honey bee colonies PLoS ONE 7 2012 e43562
48. W.A. Miller, J. Carrillo-Tripp, B.C. Bonning, A.D. Dolezal, and A.L. Toth Conclusive evidence of replication of a plant virus in honeybees is lacking mBio 5 2014 e00985-e00914
49. J.L. Li, R.S. Cornman, J.D. Evans, J.S. Pettis, Y. Zhao, C. Murphy, W.J. Peng, J. Wu, M. Hamilton, and H.F. Boncristiani et al. Reply to "Conclusive evidence of replication of a plant virus in honeybees is lacking" mBio 5 2014 e01250-e01214
50. E.-D. Ammar, C.-W. Tsai, A.E. Whitfield, M.G. Redinbaugh, and S.A. Hogenhout Cellular and molecular aspects of Rhabdovirus interactions with insect and plant hosts Ann Rev Entomol 54 2004 447 468
51. A.E. Whitfield, D.E. Ullman, and T.L. German Tospovirus-thrips interactions Annu Rev Phytopathol 43 2005 459 489
52. K.S. Mann, and R.G. Dietzgen Plant rhabdoviruses: new insights and research needs in the interplay of negative-strand RNA viruses with plant and insect hosts Arch Virol 159 2014 1889 1900
53. A.G. Power Insect transmission of plant viruses: a constraint on virus variability Curr Opin Plant Biol 3 2000 336 340
54. S.D. Card, M.N. Pearson, and G.R.G. Clover Plant pathogens transmitted by pollen Austral Plant Pathol 36 2007 455 461
55. A.M. Childress Bee-mediated transmission of blueberry leaf mottle virus via infected pollen in highbush blueberry Phytopathology 77 1987 167 172
56. P.R. Bristow, and R.R. Martin Transmission and the role of honey bees in field spread of blueberry shock ilarvirus, a pollen-borne virus of highbush blueberry Phytopathology 89 1999 124 130
57. L. Bailey, A.J. Gibbs, and R.D. Woods Two viruses from adult honey bees (Apis mellifera Linnaeus) Virology 21 1963 390 395
58. L. Bailey The purification and properties of chronic bee-paralysis virus J Gen Virol 2 1968 251 260
59. M. Allen, B.V. Ball, R.F. White, and J.F. Antoniw The detection of acute paralysis virus in Varroa jacobsoni by the use of a simple indirect ELISA J Apicult Res 25 1986 100 105
60. B.V. Ball The association of Varroa jacobsoni with virus diseases of honey bees Exp Appl Acarol 19 1983 607 613
61. B.V. Ball Acute paralysis virus isolates from honeybee, Apis mellifera, colonies infested with Varroa jacobsoni J Apicult Res 24 1985 115 119
62. B.V. Ball Varroa jacobsoni as a virus vector R. Cavalloro, Present Status of Varroatosis in Europe and Progress in the Varroa Mite Control 1989 Bernan Press 241 244
63. B.V. Ball Honey bee viruses: a cause for concern? Bee World 77 1996 117 119
64. B.V. Ball The damaging effects of Varroa jacobsoni A. Matheson, In Living with Varroa 1993 International Bee Research Association 9 16
65. B.V. Ball, and M.E. Allen The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni Annals Appl Biol 113 1988 237 244
66. L. Bailey, and B.V. Ball Honey Bee Pathology 1991 Academic Press New York, London
67. N. Möckel, S. Gisder, and E. Genersch Horizontal transmission of deformed wing virus (DWV): pathological consequences in adult bees (Apis mellifera) depend on the transmission route J Gen Virol 92 2011 370 377
68. X. Yang, and D. Cox-Foster Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge Parasitology 134 2007 405 412
69. S. Gisder, P. Aumeier, and E. Genersch Deformed wing virus (DWV): viral load and replication in mites (Varroa destructor) J Gen Virol 90 2009 463 467
70. J. Iqbal, and U. Mueller Virus infection causes specific learning deficits in honeybee foragers Proc R Soc B 274 2007 1517 1521
71. J. Moore, A. Jironkin, D. Chandler, N. Burroughs, D.J. Evans, and E.V. Ryabov Recombinants between deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies J Gen Virol 92 2011 156 161
72. E.V. Ryabov, G.R. Wood, J.M. Fannon, J.D. Moore, J.C. Bull, D. Chandler, A. Mead, N. Burroughs, and D.J. Evans A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission PLoS Path 10 2014 e1004230
73. S.D. Desai, Y.-J. Eu, S. Whyard, and R.W. Currie Reduction in deformed wing virus infection in larval and adult honey bees (Apis mellifera L.) by double-stranded RNA ingestion Insect Mol Biol 21 2012 446 455
74. C. Schöning, S. Gisder, S. Geiselhardt, I. Kretschmann, K. Bienefeld, M. Hilker, and E. Genersch Evidence for damage-dependent hygienic behaviour towards Varroa destructor parasitised brood in the western honey bee, Apis mellifera J Exp Biol 215 2012 264 271
75. Y.P. Chen, J.A. Higgins, and M.F. Feldlaufer Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.) Appl Environ Microbiol 71 2005 436 441
76. G. Di Prisco, F. Pennachio, E. Caprio, H.F. Boncristiani, J.D. Evans, and Y. Chen Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera J Gen Virol 92 2011 151 155
77. E. Maori, S. Lavi, R. Mozes-Koch, Y. Gantman, O. Edelbaum, E. Tanne, and I. Sela Isolation and characterization of IAPV, a dicistrovirus affecting honeybees in Israel: evidence for intra- and inter-species recombination J Gen Virol 88 2007 34-28-3438
78. H.F. Boncristiani, J.D. Evans, Y. Chen, J. Pettis, C. Murphy, D.L. Lopez, M. Simone-Finstrom, M. Strand, D.R. Tarpy, and O. Rueppell In vitro infection of pupae with Israeli acute paralysis virus suggests disturbance of transcriptional homeostasis in honey bees (Apis mellifera) PLoS ONE 8 2013 e73429
79. Z. Li, Y. Chen, S. Zhang, S. Chen, W. Li, L. Yan, L. Shi, L. Wu, A. Sohr, and S. Su Viral infection affects sucrose responsiveness and homing ability of forager honey bees, Apis mellifera L. PLoS ONE 8 2013 e77354
80. Y.P. Chen, J.S. Pettis, M. Corona, W.P. Chen, C.J. Li, M. Spivak, P.K. Visscher, G. DeGrandi-Hoffman, H. Boncristiani, and Y. Zhao et al. Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health PLoS Pathog 10 2014 e1004261
81. M.B. Kingsolver, Z. Huang, and R.W. Hardy Insect antiviral innate immunity: pathways, effectors, and connections J Mol Biol 425 2013 4921 4936
82. E. Maori, N. Paldi, S. Shafir, H. Kalev, E. Tsur, E. Glick, and I. Sela IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion Insect Mol Biol 18 2009 55 60
83. W. Hunter, J. Ellis, D. vanEngelsdorp, J. Hayes, D. Westervelt, E. Glick, M. Williams, I. Sela, E. Maori, and J. Pettis et al. Large-scale field application of RNAi technology reducing Israeli acute paralysis virus disease in honey bees (Apis mellifera, Hymenoptera: Apidae) PLoS Path 6 2010 e1001160
84. M.L. Flenniken, and R. Andino Non-specific dsRNA-mediated antiviral response in the honey bee PLoS ONE 8 2013 e77623
85. C. Yue, and E. Genersch RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor) J Gen Virol 86 2005 3419 3424
86. S.J. Martin, A.C. Highfield, L. Brettell, E.M. Villalobos, G.E. Budge, M. Powell, S. Nikaido, and D.C. Schroeder Global honey bee viral landscape altered by a parasitic mite Science 336 2012 1304 1306
87. J.R. Ongus, D. Peters, J.-M. Bonmatin, E. Bengsch, J.M. Vlak, and M.M. van Oers Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor J Gen Virol 85 2004 3747 3755