Honey bee pathology: Current threats to honey bees and beekeeping

Applied Microbiology and Biotechnology

Volumn 87, Issue 1, 2010, Pages 87-97

  Genersch, Elke ^a  

^a Institute for Bee Research   (Germany)

Author keywords

Colony losses; European Foulbrood; Honey bees; Nosema; Varroa; Virus

Indexed keywords

EUROPEAN FOULBROOD; FOOD PRODUCTION; FOOD SECURITY; HONEY BEE; HONEY BEES; RESEARCH ACTIVITIES; SUSTAINABLE AGRICULTURE;

AGRICULTURE; BIODIVERSITY;

VIRUSES;

ALTERNATIVE AGRICULTURE; APICULTURE; FOOD PRODUCTION; FOOD SECURITY; FUNGUS; HONEYBEE; PARASITE; PATHOLOGY; POLLINATION; POLLINATOR; REPRODUCTIVE PRODUCTIVITY; VIRUS;

APICULTURE; BACTERIAL VIRULENCE; FOOD INDUSTRY; FOOD SECURITY; HONEYBEE; POLLINATION; POLLINATOR; REPRODUCTION; SHORT SURVEY; ANIMAL; BEE; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; VIROLOGY;

ANIMALS; BEEKEEPING; BEES; POLLINATION;

ANIMALIA; APIS MELLIFERA; APOIDEA; NOSEMA; VARROA;

EID: 77952891290     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-010-2573-8     Document Type: Short Survey

References (137)

1. MA Aizen LD Harder 2009 The global stock of domesticated honey bees is growing slower than agricultural demand for pollination Curr Biol 19 915 918 1:CAS:528:DC%2BD1MXntVGjurk%3D
2. M Aizen L Garibaldi S Cunningham A Klein 2008 Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency Curr Biol 18 1572 1575 1:CAS:528:DC%2BD1cXhtlSgsbbK
3. MF Allen BV Ball 1996 The incidence and world distribution of honey bee viruses Bee World 77 141 162
4. M Allen BV Ball RF White JF Antoniw 1986 The detection of acute paralysis virus in Varroa jacobsoni by the use of a simple indirect ELISA J Apicult Res 25 100 105
5. MH Allsopp WJ de Lange R Veldtman 2008 Valuing insect pollination services with cost of replacement PloS ONE 3 e3128
6. DL Anderson 1988 Pathologist report N Z Beekeep 199 12 15
7. DL Anderson 2000 Variation in the parasitic bee mite Varroa jacobsoni Oud Apidologie 31 281 292
8. DL Anderson JWH Trueman 2000 Varroa jacobsoni (Acari: Varroidae) is more than one species Exp Appl Acarol 24 165 189 1:CAS:528:DC%2BD3cXlvVOqsLY%3D
9. A Ashiralieva E Genersch 2006 Reclassification, genotypes, and virulence of Paenibacillus larvae, the etiological agent of American foulbrood in honeybees-a review Apidologie 37 411 420
10. L Bailey 1956 Aetiology of European foulbrood: a disease of the larval honeybee Nature 178 1130
11. L Bailey 1957 The isolation and cultural characteristics of Streptococcus pluton and further observations on "Bacterium eurydice" J Gen Microbiol 17 39 48 1:CAS:528:DyaG2sXptF2itA%3D%3D
12. L Bailey 1960 The epizootiology of European foulbrood of the larval honey bee Apis mellifera L J Insect Pathol 2 67 83
13. L Bailey 1964 Acute infection of bees with paralysis virus J Insect Pathol 6 395 407 1:CAS:528:DyaF2MXltVWnsbg%3D
14. L Bailey 1965 The occurence of chronic and acute bee paralysis viruses in bees outside Britain J Invertebr Pathol 7 167 169 1:STN:280: DyaF28%2FgsVKjuw%3D%3D
15. L Bailey 1967 Acute bee-paralysis virus in adult honey bees injected with sacbrood virus Virology 33 368 1:STN:280:DyaF1c%2FhtFyisQ%3D%3D
16. L Bailey 1975 Recent research on honey bee viruses Bee World 56 55 64
17. L Bailey 1983 Melissococcus pluton, the cause of European foulbrood of honeybees (Apis ssp.) J Appl Bacteriol 55 65 69
18. Bailey L, Ball BV (1991) Honey bee pathology. Academic Press, New York
19. L Bailey MD Collins 1982 Reclassification of 'Streptococcus pluton' (White) in a new genus Melissococcus, as Melissococcus pluton nom. rev.; comb. nov J Appl Bacteriol 53 215 217
20. L Bailey AJ Gibbs RD Woods 1963 Two viruses from adult honey bees (Apis mellifera Linnaeus) Virol 21 390 395 1:STN:280:DyaF2c%2FjvFSjtw%3D%3D
21. L Bailey BV Ball JN Perry 1981 The prevalence of viruses of honey bees in Britain Ann Appl Biol 97 109 118
22. BV Ball 1983 The association of Varroa jacobsoni with virus diseases of honey bees Exp Appl Acarol 19 607 613
23. BV Ball 1985 Acute paralysis virus isolates from honeybee, Apis mellifera, colonies infested with Varroa jacobsoni J Apicult Res 24 115 119 1:CAS:528:DyaL28XjtFCgtQ%3D%3D
24. Ball BV (1989) Varroa jacobsoni as a virus vector. In: Cavalloro R (ed) Present status of varroatosis in Europe and progress in the varroa mite control. Office for Official Publications of the European Communities, Luxembourg
25. Ball BV (1993) The damaging effects of Varroa jacobsoni. In: Matheson A (ed) Living with Varroa. International Bee Research Association, Cardiff, pp 9-16
26. BV Ball 1996 Honey bee viruses: a cause for concern? Bee World 77 117 119
27. BV Ball ME Allen 1988 The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni Annals Appl Biol 113 237 244
28. Becnel JJ, Andreadis TG (1999) Microsporidia in insects. In: Witter M, Weiss LM (eds) The microsporidia and microsporidiosis. American Society of Microbiology Press, Washington, DC, pp 447-501
29. L Bekesi BV Ball M Dobos-Kovacs T Bakonyi M Rusvai 1999 Occurrence of acute paralysis virus of the honey bee (Apis mellifera) in a Hungarian apiary infested with the parasitic mite Varroa jacobsoni Acta Vet Hung 47 319 324 1:STN:280:DyaK1MvislCktw%3D%3D (Pubitemid 129602391)
30. O Berenyi T Bakonyi I Derakhshifar H Köglberger N Nowotny 2006 Occurence of six honeybee viruses in diseased Austrian apiaries Appl Environ Microbiol 72 2414 2420 1:CAS:528:DC%2BD28XktFagtLo%3D
31. E Bigliardi L Sacchi 2001 Cell biology and invasion of the microsporidia Microbes Infect 3 373 379 1:STN:280:DC%2BD3M3nslejsA%3D%3D
32. O Boecking E Genersch 2008 Varroosis-the ongoing crisis in bee keeping J Verbr Lebensm 3 221 228
33. PL Bowen-Walker SJ Martin A Gunn 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
34. J Cai MD Collins 1994 Evidence for a close phylogenetic relationship between Melissococcus pluton, the causative agent of European Foulbrood disease, and the genus Enterococcus Int J Syst Bacteriol 44 365 367 1:CAS:528: DyaK2cXlt12ks7o%3D
35. Canning EU, Lom J (1986) The microsporidia of vertebrates. Academic Press, New York, pp 1-16
36. MP Chauzat M Higes R Martin-Hernandez A Meana N Cougoule JP Faucon 2007 Presence of Nosema ceranae in French honey bee colonies J Apicult Res 46 127 128
37. Chen YP, Evans JD (2007) Historical presence of Israeli acute paralysis virus in the United States. Am. Bee J
38. Y-P Chen R Siede 2007 Honey bee viruses Adv Virus Res 70 33 80 1:CAS:528:DC%2BD1cXhs1ajur0%3D
39. Y Chen JD Evans IB Smith JS Pettis 2008 Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States J.Invertebr Pathol 97 186 188
40. YP Chen JD Evans C Murphy R Gutell M Zuker D Gundensen-Rindal JS Pettis 2009 Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera J Eukaryot Microbiol 56 142 147 1:CAS:528:DC%2BD1MXltlymt7c%3D
41. D Cox-Foster D VanEngelsdorp 2009 Saving the honeybee Sci Am 300 40 47
42. DL Cox-Foster S Conlan EC Holmes G Palacios JD Evans NA Moran P-L Quan S Briese M Hornig DM Geiser V Martinson D vanEngelsdorp AL Kalkseitn L Drysdale J Hui J Zhai L Cui S Hutchison JF Simons M Egholm JS Pettis WI Lipkin 2007 A metagenomic survey of microbes in honey bee colony collapse disorder Science 318 283 287 1:CAS:528:DC%2BD2sXhtFCjt7vM
43. LI De Guzman M Delfinado-Baker 1996 A new species of Varroa (Acari: Varroidae) associated with Apis koschevnikovi (Apidae: Hymenoptera) in Borneo Int J Acarol 22 23 27
44. D De Jong PH De Jong LS Gonçalves 1982 Weight loss and other damage to developing worker honeybees from infestation with V. jacobsoni J Apicult Res 21 165 216
45. JR de Miranda I Fries 2008 Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.) J Invertebr Pathol 98 184 189
46. JR de Miranda E Genersch 2010 Deformed wing virus J Invertebr Pathol 103 S48 S61
47. J de Miranda G Cordoni G Budge 2010 The acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex J Invertebr Pathol 103 S30 S47
48. KS Delaplane WM Hood 1999 Economic threshold for Varroa jacobsoni Oud. in the southeastern USA Apidologie 30 383 395
49. M Delfinado-Baker K Aggarwal 1987 A new Varroa (Acari: Varroidae) from the nest of Apis cerana (Apidae) Int J Acarol 13 233 237
50. SP Djordjevic K Noone L Smith MAZ Hornitzky 1998 Development of a hemi-nested PCR assay for the specific detection of Melissococcus pluton J Apicult Res 37 165 174
51. P Duay D de Jong W Engels 2002 Decreased flight performance and sperm production in drones of the honey bee (Apis mellifera) slightly infested by Varroa destructor mites during pupal development Genet Mol Res 1 227 232
52. P Duay D de Jong W Engels 2003 Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites Apidologie 34 61 65
53. JD Evans 2006 Beepath: an ordered quantitative-PCR array for exploring honey bee immunity and disease J Invertebr Pathol 93 135 139 1:CAS:528:DC%2BD28XhtVajsLrF
54. S Fenoy C Rueda M Higes R Martín-Hernandez C del Aguila 2009 High-level resistance of Nosema ceranae, a parasite of the honeybee, to temperature and desiccation Appl Environ Microbiol 75 6886 6889 1:CAS:528:DC%2BD1MXhsVGrs77K
55. E Forsgren 2010 European foulbrood in honey bees J Invertebr Pathol 103 S5 S9
56. E Forsgren AC Lundhagen A Imdorf I Fries 2005 Distribution of Melissococcus plutonius in honeybee colonies with and without symptoms of European foulbrood Microbial Ecol 50 369 374
57. C Franzen 2005 How do microsporidia invade cells? Folia Parasitol 52 36 40
58. I Fries 1988 Infectivity and multiplication of Nosema apis Z. in the ventriculus of the honey bee Apidologie 19 319 328
59. I Fries 2010 Nosema ceranae in European honey bees (Apis mellifera) J Invertebr Pathol. 103 Suppl 1 S73 S79
60. I Fries S Camazine J Sneyd 1994 Population dynamics of Varroa jacobsoni: a model and a review Bee World 75 5 28
61. I Fries F Feng A daSilva SB Slemenda NJ Pieniazek 1996 Nosema ceranae n sp (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae) Eur J Protistol 32 356 365
62. I Fries R Martin A Meana P Garcia-Palencia M Higes 2006 Natural infections of Nosema ceranae in European honey bees J Apicult Res 45 230 233
63. L Gauthier D Tentcheva M Tournaire B Dainat F Cousserans ME Colin M Bergoin 2007 Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique Apidologie 38 426 435 1:CAS:528: DC%2BD1cXhvV2gtg%3D%3D
64. E Genersch 2007 Paenibacillus larvae and American foulbrood in honeybees Berl Münch Tierärztl Wschr 120 26 33
65. E Genersch 2008 Paenibacillus larvae and American foulbrood-long since known and still surprising J Verbr Lebensm 3 429 434
66. E Genersch 2010 American Foulbrood in honeybees and its causative agent, Paenibacillus larvae J Invertebr Pathol 103 S10 S19
67. E Genersch E Forsgren J Pentikäinen A Ashiralieva S Rauch J Kilwinski I Fries 2006 Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation Int J Syst Evol Microbiol 56 501 511 1:CAS:528:DC%2BD28XjslCkurc%3D
68. Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C, Büchler R, Berg S, Ritter W, Mühlen W, Gisder S, Meixner M, Liebig G, Rosenkranz P (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie. doi: 10.1051/apido/2010014
69. J Ghazoul 2005 Buzziness as usual? Questioning the global pollination crisis Trends Ecol Evol 20 367 373
70. J Ghazoul 2005 Response to Steffan-Dewenter et al.: questioning the global pollination crisis Trends Ecol Evol 20 652 653
71. T Giersch T Berg F Galea M Hornitzky 2009 Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia Apidologie 40 117 123 1:CAS:528:DC%2BD1MXmtVShsbw%3D
72. S Gisder P Aumeier E Genersch 2009 Deformed wing virus (DWV): viral load and replication in mites (Varroa destructor) J Gen Virol 90 463 467 1:CAS:528:DC%2BD1MXhslejtLs%3D
73. Gisder S, Hedtke K, Möckel N, Frielitz M-C, Linde A, Genersch E (2010) Five-year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae? Appl Environ Microbiol. doi: 10.1128/AEM.03097-09
74. VA Govan V Brozel MH Allsopp S Davison 1998 A PCR detection method for rapid identification of Melissococcus pluton in honeybee larvae Appl Environ Microbiol 64 1983 1985 1:CAS:528:DyaK1cXislWlt74%3D
75. PG Gregory JD Evans TE Rinderer L de Guzman 2005 Conditional immune gene suppression of honeybees parasitized by Varroa mites J Insect Sci 5 1 5
76. E Guzmán-Novoa L Eccles Y Calvete J Mcgowan PG Kelly A Correa-Benítez 2010 Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada Apidologie 10.1051/apido/2009076
77. Hails RS, Ball BV, Genersch E (2007) Infection strategies of insect viruses. In: Aubert M et al. (eds) Virology and the Honey Bee. European Communities, Luxembourg, pp. 255-275
78. M Higes R Martin A Meana 2006 Nosema ceranae, a new microsporidian parasite in honeybees in Europe J Invertebr Pathol 92 93 95 1:CAS:528: DC%2BD28XkvVGjtb0%3D
79. M Higes P Garcia-Palencia R Martin-Hernandez A Meana 2007 Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia) J Invertebr Pathol 94 211 217
80. M Higes R Martín-Hernández C Botías E Garrido Bailón AV González-Porto L Barrios MJ del Nozal JL Bernal JJ Jiménez P García Palencia A Meana 2008 How natural infection by Nosema ceranae causes honeybee colony collapse Environ Microbiol 10 2659 2669
81. M Higes R Martin-Hernandez E Garrido-Bailon P Garcia-Palencia A Meana 2008 Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees J Invertebr Pathol 97 76 78
82. WF Huang JH Jiang YW Chen CH Wang 2007 A Nosema ceranae isolate from the honeybee Apis mellifera Apidologie 38 30 37
83. ACF Hung JR Adams H Shimanuki 1995 Bee parasitic mite syndrome: II. The role of Varroa mite and viruses Am Bee J 135 702
84. AC Hung H Shimanuki DA Knox 1996 Inapparent infection of acute paralysis virus and Kashmir bee virus in the U.S. honey bees Am Bee J 136 874 876
85. AC Hung H Shimanuki DV Knox 1996 The role of viruses in bee parasitic mite syndrome Am Bee J 136 731 732
86. ACF Hung BV Ball JR Adams H Shimanuki DA Knox 1996 A scientific note on the detection of American strains of acute paralysis virus and Kashmir bee virus in dead bees in one US honey bee (Apis mellifera L.) colony Apidologie 27 55 56
87. C Invernizzi C Abud IH Tomasco J Harriet G Ramallo J Campá H Katz G Gardiol Y Mendoza 2009 Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay J Invertebr Pathol 101 150 153
88. J Klee AM Besana E Genersch S Gisder A Nanetti DQ Tam TX Chinh F Puerta JM Ruz P Kryger D Message F Hatjina S Korpela I Fries RJ Paxton 2007 Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera J Invertebr Pathol 96 1 10
89. A-M Klein BE Vaissiere JH Cane I Steffan-Dewenter SA Cunningham C Kremen T Tscharntke 2007 Importance of pollinators in changing landscapes for world crops Proc R Soc B 274 303 313
90. W Koch W Ritter 1991 Experimental examinations concerning the problem of deformed emerging bees after infestation with Varroa jacobsoni J Vet Med B 38 337 344 1:STN:280:DyaK38%2FisVKhsg%3D%3D
91. J Kralj S Fuchs 2006 Parasitic Varroa destructor mites influence flight duration and homing ability of infested Apis mellifera foragers Apidologie 37 577 587
92. J Kralj A Brockmann S Fuchs J Tautz 2007 The parasitic mite Varroa destructor affects non-associative learning in honey bee foragers, Apis mellifera L J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193 363 370
93. E Maori S Lavi R Mozes-Koch Y Gantman O Edelbaum E Tanne I Sela 2007 Isolation and characterization of IAPV, a dicistrovirus affecting honeybees in Israel: evidence for intra- and inter-species recombination J Gen Virol 88 3428 3438 1:CAS:528:DC%2BD2sXhsVersb%2FK
94. E Maori N Paldi S Shafir H Kalev E Tsur E Glick I Sela 2009 IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion Insect Mol Biol 18 55 60 1:CAS:528:DC%2BD1MXit1Khsbw%3D
95. J Marcangeli L Monetti N Fernandez 1992 Malformations produced by Varroa jacobsoni on Apis mellifera in the province of Buenos Aires, Argentina Apidologie 23 399 402
96. SJ Martin 2001 The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach J Appl Ecol 38 1082 1093
97. R Martin-Hernandez A Meana L Prieto AM Salvador E Garrido-Bailon M Higes 2007 Outcome of colonization of Apis mellifera by Nosema ceranae Appl Environ Microbiol 73 6331 6338 1:CAS:528:DC%2BD2sXht1ektL3E
98. R Martin-Hernandez A Meana P Garcia-Palencia P Marin C Botias E Garrido-Bailon L Barrios M Higes 2009 Effect of temperature on the biotic potential of honeybee microsporidia Appl Environ Microbiol 75 2554 2557 1:CAS:528:DC%2BD1MXlsFChsb0%3D
99. C Mayack D Naug 2009 Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection J Invertebr Pathol 100 185 188
100. M Navajas A Migeon C Alaux ML Martin-Magniette GE Robinson JD Evans S Cros-Arteil D Crauser Y Le Conte 2008 Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection BMC Genomics 9 301 1:CAS:528:DC%2BD1cXhtVWjsLrM
101. S Nordström I Fries A Aarhus H Hansen S Korpela 1999 Virus infections in Nordic honey bee colonies with no, low or severe Varroa jacobsoni infestations Apidologie 30 475 484
102. BP Oldroyd 2007 What's killing American honey bees? PLoS Biol 5 e168
103. AC Oudemans 1904 On a new genus and species of parasitic acari Notes from the Leyden Museum 24 216 222
104. G Palacios J Hui PL Quan A Kalkstein KS Honkavuori AV Bussetti S Conlan J Evans YP Chen D van Engelsdorp H Efrat J Pettis D Cox-Foster EC Holmes T Briese WI Lipkin 2008 Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States J Virol 82 6209 6217 1:CAS:528:DC%2BD1cXnslyrt7s%3D
105. RJ Paxton J Klee S Korpela I Fries 2007 Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis Apidologie 38 558 565
106. FLW Ratnieks NL Carreck 2010 Clarity on honey bee collapse? Science 327 152 153 1:CAS:528:DC%2BC3cXosFGgtw%3D%3D
107. M Ribière V Olivier P Blanchard 2010 Chronic bee paralysis: a disease and a virus like no other? J Invertebr Pathol 103 S120 S31
108. AJ Richards 2001 Does low biodiversity resulting from modern agriculture practice affect crop pollination and yield? Ann Bot 88 165 172
109. W Ritter E Leclercq W Koch 1984 Observation des populations d'abeilles et de Varroa dans les colonies à différents niveaux d'infestation Apidologie 15 389 400
110. A Roetschi H Berthoud R Kuhn A Imdorf 2008 Infection rate based on quantitative real-time PCR of Melissococcus plutonius, the causal agent of European foulbrood, in honeybee colonies before and after apiary sanitation Apidologie 39 362 371 1:CAS:528:DC%2BD1cXosFSls7k%3D
111. P Rosenkranz P Aumeier B Ziegelmann 2010 Biology and control of Varroa destructor J Invertebr Pathol 103 S96 S119
112. H Shimanuki NW Calderone DA Knox 1994 Parasitic mite syndrome: the symptoms Am Bee J 134 827 828
113. R Siede M König R Büchler K Failing H-J Thiel 2008 A real-time PCR based survey on acute bee paralysis virus in German bee colonies Apidologie 39 650 661 1:CAS:528:DC%2BD1MXivFWjt70%3D
114. M Solignac D Vautrin A Pizzo M Navajas Y Le Conte JM Cornuet 2003 Characterization of microsatellite markers from the apicultural pest Varroa destructor (Acari: Varroidae) and its relatives Mol Ecol Notes 3 556 559 1:CAS:528:DC%2BD2cXks12mug%3D%3D
115. M Solignac J-M Cornuet D Vautrin Y Le Conte DL Anderson JD Evans S Cros-Arteil M Navajas 2005 The invasive Korea and Japan types of Varroa destructor, ectoparasitic mites of the Western honey bee (Apis mellifera), are two partly isolated clones Proc Roy Soc Lond Ser B: Biol Sci 272 411 419
116. I Steffan-Dewenter SG Potts L Packer 2005 Pollinator diversity and crop pollination services are at risk Trends Ecol Evol 20 651 652
117. DA Sumner H Boriss 2006 Bee-economics and the leap in pollination fees. ARE update. Giannini Found Agric Econ 9 9 12
118. Z Tapaszti P Forgách C Kovágó L Békési T Bakonyi M Rusvai 2009 First detection and dominance of Nosema ceranae in Hungarian honeybee colonies Acta Vet Hung 57 383 388
119. D Tentcheva L Gauthier N Zappulla B Dainat F Cousserans ME Colin M Bergoin 2004 Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France Appl Environ Microbiol 70 7185 7191 1:CAS:528:DC%2BD2cXhtFaitr%2FP
120. JH Todd JR De Miranda BV Ball 2007 Incidence and molecular characterization of viruses found in dying New Zealand honey bee (Apis mellifera) colonies infested with Varroa destructor Apidologie 38 354 367 1:CAS:528:DC%2BD1cXjsVeisQ%3D%3D
121. HG Truper L dé Clari 1998 Taxonomic note: erratum and correction of further specific epithets formed as sustantives (nouns) in apposition Int J Syst Bacteriol 48 615
122. D vanEngelsdorp MD Meixner 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
123. D vanEngelsdorp R Underwood D Caron J Hayes 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
124. D vanEngelsdorp J Hayes Jr RM Underwood J Pettis 2008 A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008 PLoS ONE 3 e4071
125. D vanEngelsdorp JD Evans C Saegerman C Mullin E Haubruge BK Nguyen M Frazier J Frazier D Cox-Foster Y Chen R Underwood DR Tarpy JS Pettis 2009 Colony collapse disorder: a descriptive study PLoS One 4 8 e6481
126. R Weber RT Bryan DA Schwartz RL Owen 1994 Human microsporidial infections Clin Microbiol Rev 7 426 461 1:STN:280:DyaK2M7js1ajsQ%3D%3D
127. GF White 1906 The bacteria of the apiary with special reference to bee disease USDA, Bureau of Entomology, Technical Series 14 1 50
128. White GF (1912) The cause of European foulbrood. US Department of Agriculture Bureau of Entomology Circular No. 157. US Department of Agriculture, Washington
129. Wiegers FP (1988) Transmission of honeybee viruses by Varroa jacobsoni Oud. In: Cavalloro R (ed) European research on varroatosis control. A. A. Balkema Publishers, Rotterdam, pp 99-104
130. S Wilkins M Brown A Andrew GS Cuthbertson 2007 The incidence of honey bee pests and diseases in England and Wales Pest Manag Sci 63 1062 1068 1:CAS:528:DC%2BD2sXht1KntrjL
131. GR Williams ABA Shafer REL Rogers D Shutler DT Stewart 2008 First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA J Invertebr Pathol 97 189 192
132. X Yang DL Cox-Foster 2005 Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification Proc Natl Acad Sci USA 102 7470 7475 1:CAS:528: DC%2BD2MXkslOnt7k%3D
133. X Yang D Cox-Foster 2007 Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge Parasitology 134 405 412 1:STN:280:DC%2BD2s%2FmtVKqtQ%3D%3D
134. C Yue E Genersch 2005 RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor) J Gen Virol 86 3419 3424 1:CAS:528:DC%2BD2MXht12ntLzI
135. C Yue M Schröder K Bienefeld E Genersch 2006 Detection of viral sequences in semen of honeybees (Apis mellifera): evidence for vertical transmission of viruses through drones J Invertebr Pathol 92 93 96
136. C Yue M Schröder S Gisder E Genersch 2007 Vertical transmission routes for deformed wing virus of honeybees (Apis mellifera) J Gen Virol 88 2329 2336 1:CAS:528:DC%2BD2sXpsFejt7w%3D
137. E Zander 1909 Tierische Parasiten als Krankheitserreger bei der Biene Münchener Bienenzeitung 31 196 204