Applied Microbiology and Biotechnology

, Volume 87, Issue 1, pp 87–97 | Cite as

Honey bee pathology: current threats to honey bees and beekeeping

Mini-Review

Abstract

Managed honey bees are the most important commercial pollinators of those crops which depend on animal pollination for reproduction and which account for 35% of the global food production. Hence, they are vital for an economic, sustainable agriculture and for food security. In addition, honey bees also pollinate a variety of wild flowers and, therefore, contribute to the biodiversity of many ecosystems. Honey and other hive products are, at least economically and ecologically rather, by-products of beekeeping. Due to this outstanding role of honey bees, severe and inexplicable honey bee colony losses, which have been reported recently to be steadily increasing, have attracted much attention and stimulated many research activities. Although the phenomenon “decline of honey bees” is far from being finally solved, consensus exists that pests and pathogens are the single most important cause of otherwise inexplicable colony losses. This review will focus on selected bee pathogens and parasites which have been demonstrated to be involved in colony losses in different regions of the world and which, therefore, are considered current threats to honey bees and beekeeping.

Keywords

Honey bees Varroa Virus Nosema European Foulbrood Colony losses 

References

  1. Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918CrossRefGoogle Scholar
  2. Aizen M, Garibaldi L, Cunningham S, Klein A (2008) Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr Biol 18:1572–1575CrossRefGoogle Scholar
  3. Allen MF, Ball BV (1996) The incidence and world distribution of honey bee viruses. Bee World 77:141–162Google Scholar
  4. Allen M, Ball BV, White RF, Antoniw JF (1986) The detection of acute paralysis virus in Varroa jacobsoni by the use of a simple indirect ELISA. J Apicult Res 25:100–105Google Scholar
  5. Allsopp MH, de Lange WJ, Veldtman R (2008) Valuing insect pollination services with cost of replacement. PloS ONE 3:e3128CrossRefGoogle Scholar
  6. Anderson DL (1988) Pathologist report. N Z Beekeep 199:12–15Google Scholar
  7. Anderson DL (2000) Variation in the parasitic bee mite Varroa jacobsoni Oud. Apidologie 31:281–292CrossRefGoogle Scholar
  8. Anderson DL, Trueman JWH (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp Appl Acarol 24:165–189CrossRefGoogle Scholar
  9. Ashiralieva A, Genersch E (2006) Reclassification, genotypes, and virulence of Paenibacillus larvae, the etiological agent of American foulbrood in honeybees—a review. Apidologie 37:411–420CrossRefGoogle Scholar
  10. Bailey L (1956) Aetiology of European foulbrood: a disease of the larval honeybee. Nature 178:1130CrossRefGoogle Scholar
  11. Bailey L (1957) The isolation and cultural characteristics of Streptococcus pluton and further observations on “Bacterium eurydice”. J Gen Microbiol 17:39–48Google Scholar
  12. Bailey L (1960) The epizootiology of European foulbrood of the larval honey bee Apis mellifera L. J Insect Pathol 2:67–83Google Scholar
  13. Bailey L (1964) Acute infection of bees with paralysis virus. J Insect Pathol 6:395–407Google Scholar
  14. Bailey L (1965) The occurence of chronic and acute bee paralysis viruses in bees outside Britain. J Invertebr Pathol 7:167–169CrossRefGoogle Scholar
  15. Bailey L (1967) Acute bee-paralysis virus in adult honey bees injected with sacbrood virus. Virology 33:368CrossRefGoogle Scholar
  16. Bailey L (1975) Recent research on honey bee viruses. Bee World 56:55–64Google Scholar
  17. Bailey L (1983) Melissococcus pluton, the cause of European foulbrood of honeybees (Apis ssp.). J Appl Bacteriol 55:65–69Google Scholar
  18. Bailey L, Ball BV (1991) Honey bee pathology. Academic Press, New YorkGoogle Scholar
  19. Bailey L, Collins MD (1982) Reclassification of ‘Streptococcus pluton’ (White) in a new genus Melissococcus, as Melissococcus pluton nom. rev.; comb. nov. J Appl Bacteriol 53:215–217Google Scholar
  20. Bailey L, Gibbs AJ, Woods RD (1963) Two viruses from adult honey bees (Apis mellifera Linnaeus). Virol 21:390–395CrossRefGoogle Scholar
  21. Bailey L, Ball BV, Perry JN (1981) The prevalence of viruses of honey bees in Britain. Ann Appl Biol 97:109–118CrossRefGoogle Scholar
  22. Ball BV (1983) The association of Varroa jacobsoni with virus diseases of honey bees. Exp Appl Acarol 19:607–613Google Scholar
  23. Ball BV (1985) Acute paralysis virus isolates from honeybee, Apis mellifera, colonies infested with Varroa jacobsoni. J Apicult Res 24:115–119Google Scholar
  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, LuxembourgGoogle Scholar
  25. Ball BV (1993) The damaging effects of Varroa jacobsoni. In: Matheson A (ed) Living with Varroa. International Bee Research Association, Cardiff, pp 9–16Google Scholar
  26. Ball BV (1996) Honey bee viruses: a cause for concern? Bee World 77:117–119Google Scholar
  27. Ball BV, Allen ME (1988) The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni. Annals Appl Biol 113:237–244CrossRefGoogle Scholar
  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 447–501Google Scholar
  29. Bekesi L, Ball BV, Dobos-Kovacs M, Bakonyi T, Rusvai M (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 47:319–324CrossRefGoogle Scholar
  30. Berenyi O, Bakonyi T, Derakhshifar I, Köglberger H, Nowotny N (2006) Occurence of six honeybee viruses in diseased Austrian apiaries. Appl Environ Microbiol 72:2414–2420CrossRefGoogle Scholar
  31. Bigliardi E, Sacchi L (2001) Cell biology and invasion of the microsporidia. Microbes Infect 3:373–379CrossRefGoogle Scholar
  32. Boecking O, Genersch E (2008) Varroosis—the ongoing crisis in bee keeping. J Verbr Lebensm 3:221–228CrossRefGoogle Scholar
  33. Bowen-Walker PL, Martin SJ, Gunn A (1999) The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J Invertebr Pathol 73:101–106CrossRefGoogle Scholar
  34. Cai J, Collins MD (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 44:365–367CrossRefGoogle Scholar
  35. Canning EU, Lom J (1986) The microsporidia of vertebrates. Academic Press, New York, pp 1–16Google Scholar
  36. Chauzat MP, Higes M, Martin-Hernandez R, Meana A, Cougoule N, Faucon JP (2007) Presence of Nosema ceranae in French honey bee colonies. J Apicult Res 46:127–128CrossRefGoogle Scholar
  37. Chen YP, Evans JD (2007) Historical presence of Israeli acute paralysis virus in the United States. Am. Bee JGoogle Scholar
  38. Chen Y-P, Siede R (2007) Honey bee viruses. Adv Virus Res 70:33–80CrossRefGoogle Scholar
  39. Chen Y, Evans JD, Smith IB, Pettis JS (2008) Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. JInvertebr Pathol 97:186–188CrossRefGoogle Scholar
  40. Chen YP, Evans JD, Murphy C, Gutell R, Zuker M, Gundensen-Rindal D, Pettis JS (2009) Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. J Eukaryot Microbiol 56:142–147CrossRefGoogle Scholar
  41. Cox-Foster D, VanEngelsdorp D (2009) Saving the honeybee. Sci Am 300:40–47CrossRefGoogle Scholar
  42. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan P-L, Briese S, Hornig M, Geiser DM, Martinson V, vanEngelsdorp D, Kalkseitn AL, Drysdale L, Hui J, Zhai J, Cui L, Hutchison S, Simons JF, Egholm M, Pettis JS, Lipkin WI (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283–287CrossRefGoogle Scholar
  43. De Guzman LI, Delfinado-Baker M (1996) A new species of Varroa (Acari: Varroidae) associated with Apis koschevnikovi (Apidae: Hymenoptera) in Borneo. Int J Acarol 22:23–27CrossRefGoogle Scholar
  44. De Jong D, De Jong PH, Gonçalves LS (1982) Weight loss and other damage to developing worker honeybees from infestation with V. jacobsoni. J Apicult Res 21:165–216Google Scholar
  45. de Miranda JR, Fries I (2008) Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J Invertebr Pathol 98:184–189CrossRefGoogle Scholar
  46. de Miranda JR, Genersch E (2010) Deformed wing virus. J Invertebr Pathol 103:S48–S61CrossRefGoogle Scholar
  47. de Miranda J, Cordoni G, Budge G (2010) The acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J Invertebr Pathol 103:S30–S47CrossRefGoogle Scholar
  48. Delaplane KS, Hood WM (1999) Economic threshold for Varroa jacobsoni Oud. in the southeastern USA. Apidologie 30:383–395CrossRefGoogle Scholar
  49. Delfinado-Baker M, Aggarwal K (1987) A new Varroa (Acari: Varroidae) from the nest of Apis cerana (Apidae). Int J Acarol 13:233–237CrossRefGoogle Scholar
  50. Djordjevic SP, Noone K, Smith L, Hornitzky MAZ (1998) Development of a hemi-nested PCR assay for the specific detection of Melissococcus pluton. J Apicult Res 37:165–174Google Scholar
  51. Duay P, de Jong D, Engels W (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 1:227–232Google Scholar
  52. Duay P, de Jong D, Engels W (2003) Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites. Apidologie 34:61–65CrossRefGoogle Scholar
  53. Evans JD (2006) Beepath: an ordered quantitative-PCR array for exploring honey bee immunity and disease. J Invertebr Pathol 93:135–139CrossRefGoogle Scholar
  54. Fenoy S, Rueda C, Higes M, Martín-Hernandez R, del Aguila C (2009) High-level resistance of Nosema ceranae, a parasite of the honeybee, to temperature and desiccation. Appl Environ Microbiol 75:6886–6889CrossRefGoogle Scholar
  55. Forsgren E (2010) European foulbrood in honey bees. J Invertebr Pathol 103:S5–S9CrossRefGoogle Scholar
  56. Forsgren E, Lundhagen AC, Imdorf A, Fries I (2005) Distribution of Melissococcus plutonius in honeybee colonies with and without symptoms of European foulbrood. Microbial Ecol 50:369–374CrossRefGoogle Scholar
  57. Franzen C (2005) How do microsporidia invade cells? Folia Parasitol 52:36–40Google Scholar
  58. Fries I (1988) Infectivity and multiplication of Nosema apis Z. in the ventriculus of the honey bee. Apidologie 19:319–328CrossRefGoogle Scholar
  59. Fries I (2010) Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 103(Suppl 1):S73–S79CrossRefGoogle Scholar
  60. Fries I, Camazine S, Sneyd J (1994) Population dynamics of Varroa jacobsoni: a model and a review. Bee World 75:5–28Google Scholar
  61. Fries I, Feng F, daSilva A, Slemenda SB, Pieniazek NJ (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 32:356–365Google Scholar
  62. Fries I, Martin R, Meana A, Garcia-Palencia P, Higes M (2006) Natural infections of Nosema ceranae in European honey bees. J Apicult Res 45:230–233Google Scholar
  63. Gauthier L, Tentcheva D, Tournaire M, Dainat B, Cousserans F, Colin ME, Bergoin M (2007) Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique. Apidologie 38:426–435CrossRefGoogle Scholar
  64. Genersch E (2007) Paenibacillus larvae and American foulbrood in honeybees. Berl Münch Tierärztl Wschr 120:26–33Google Scholar
  65. Genersch E (2008) Paenibacillus larvae and American foulbrood—long since known and still surprising. J Verbr Lebensm 3:429–434CrossRefGoogle Scholar
  66. Genersch E (2010) American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invertebr Pathol 103:S10–S19CrossRefGoogle Scholar
  67. Genersch E, Forsgren E, Pentikäinen J, Ashiralieva A, Rauch S, Kilwinski J, Fries I (2006) Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int J Syst Evol Microbiol 56:501–511CrossRefGoogle Scholar
  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. Ghazoul J (2005a) Buzziness as usual? Questioning the global pollination crisis. Trends Ecol Evol 20:367–373CrossRefGoogle Scholar
  70. Ghazoul J (2005b) Response to Steffan-Dewenter et al.: questioning the global pollination crisis. Trends Ecol Evol 20:652–653CrossRefGoogle Scholar
  71. Giersch T, Berg T, Galea F, Hornitzky M (2009) Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie 40:117–123CrossRefGoogle Scholar
  72. Gisder S, Aumeier P, Genersch E (2009) Deformed wing virus (DWV): viral load and replication in mites (Varroa destructor). J Gen Virol 90:463–467CrossRefGoogle Scholar
  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. Govan VA, Brozel V, Allsopp MH, Davison S (1998) A PCR detection method for rapid identification of Melissococcus pluton in honeybee larvae. Appl Environ Microbiol 64:1983–1985Google Scholar
  75. Gregory PG, Evans JD, Rinderer TE, de Guzman L (2005) Conditional immune gene suppression of honeybees parasitized by Varroa mites. J Insect Sci 5:1–5Google Scholar
  76. Guzmán-Novoa E, Eccles L, Calvete Y, Mcgowan J, Kelly PG, Correa-Benítez A (2010) Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie. doi:10.1051/apido/2009076 Google Scholar
  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. 255–275Google Scholar
  78. Higes M, Martin R, Meana A (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92:93–95CrossRefGoogle Scholar
  79. Higes M, Garcia-Palencia P, Martin-Hernandez R, Meana A (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J Invertebr Pathol 94:211–217CrossRefGoogle Scholar
  80. Higes M, Martín-Hernández R, Botías C, Garrido Bailón E, González-Porto AV, Barrios L, del Nozal MJ, Bernal JL, Jiménez JJ, García Palencia P, Meana A (2008a) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10:2659–2669CrossRefGoogle Scholar
  81. Higes M, Martin-Hernandez R, Garrido-Bailon E, Garcia-Palencia P, Meana A (2008b) Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. J Invertebr Pathol 97:76–78CrossRefGoogle Scholar
  82. Huang WF, Jiang JH, Chen YW, Wang CH (2007) A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38:30–37CrossRefGoogle Scholar
  83. Hung ACF, Adams JR, Shimanuki H (1995) Bee parasitic mite syndrome: II. The role of Varroa mite and viruses. Am Bee J 135:702Google Scholar
  84. Hung AC, Shimanuki H, Knox DA (1996a) Inapparent infection of acute paralysis virus and Kashmir bee virus in the U.S. honey bees. Am Bee J 136:874–876Google Scholar
  85. Hung AC, Shimanuki H, Knox DV (1996b) The role of viruses in bee parasitic mite syndrome. Am Bee J 136:731–732Google Scholar
  86. Hung ACF, Ball BV, Adams JR, Shimanuki H, Knox DA (1996c) 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 27:55–56CrossRefGoogle Scholar
  87. Invernizzi C, Abud C, Tomasco IH, Harriet J, Ramallo G, Campá J, Katz H, Gardiol G, Mendoza Y (2009) Presence of Nosema ceranae in honeybees (Apis mellifera) in Uruguay. J Invertebr Pathol 101:150–153CrossRefGoogle Scholar
  88. Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, Tam DQ, Chinh TX, Puerta F, Ruz JM, Kryger P, Message D, Hatjina F, Korpela S, Fries I, Paxton RJ (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96:1–10CrossRefGoogle Scholar
  89. Klein A-M, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313CrossRefGoogle Scholar
  90. Koch W, Ritter W (1991) Experimental examinations concerning the problem of deformed emerging bees after infestation with Varroa jacobsoni. J Vet Med B 38:337–344CrossRefGoogle Scholar
  91. Kralj J, Fuchs S (2006) Parasitic Varroa destructor mites influence flight duration and homing ability of infested Apis mellifera foragers. Apidologie 37:577–587CrossRefGoogle Scholar
  92. Kralj J, Brockmann A, Fuchs S, Tautz J (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 193:363–370CrossRefGoogle Scholar
  93. Maori E, Lavi S, Mozes-Koch R, Gantman Y, Edelbaum O, Tanne E, Sela I (2007) Isolation and characterization of IAPV, a dicistrovirus affecting honeybees in Israel: evidence for intra- and inter-species recombination. J Gen Virol 88:3428–3438CrossRefGoogle Scholar
  94. Maori E, Paldi N, Shafir S, Kalev H, Tsur E, Glick E, Sela I (2009) IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion. Insect Mol Biol 18:55–60CrossRefGoogle Scholar
  95. Marcangeli J, Monetti L, Fernandez N (1992) Malformations produced by Varroa jacobsoni on Apis mellifera in the province of Buenos Aires, Argentina. Apidologie 23:399–402CrossRefGoogle Scholar
  96. Martin SJ (2001) The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J Appl Ecol 38:1082–1093CrossRefGoogle Scholar
  97. Martin-Hernandez R, Meana A, Prieto L, Salvador AM, Garrido-Bailon E, Higes M (2007) Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 73:6331–6338CrossRefGoogle Scholar
  98. Martin-Hernandez R, Meana A, Garcia-Palencia P, Marin P, Botias C, Garrido-Bailon E, Barrios L, Higes M (2009) Effect of temperature on the biotic potential of honeybee microsporidia. Appl Environ Microbiol 75:2554–2557CrossRefGoogle Scholar
  99. Mayack C, Naug D (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol 100:185–188CrossRefGoogle Scholar
  100. Navajas M, Migeon A, Alaux C, Martin-Magniette ML, Robinson GE, Evans JD, Cros-Arteil S, Crauser D, Le Conte Y (2008) Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 9:301CrossRefGoogle Scholar
  101. Nordström S, Fries I, Aarhus A, Hansen H, Korpela S (1999) Virus infections in Nordic honey bee colonies with no, low or severe Varroa jacobsoni infestations. Apidologie 30:475–484CrossRefGoogle Scholar
  102. Oldroyd BP (2007) What's killing American honey bees? PLoS Biol 5:e168CrossRefGoogle Scholar
  103. Oudemans AC (1904) On a new genus and species of parasitic acari. Notes from the Leyden Museum 24:216–222Google Scholar
  104. Palacios G, Hui J, Quan PL, Kalkstein A, Honkavuori KS, Bussetti AV, Conlan S, Evans J, Chen YP, van Engelsdorp D, Efrat H, Pettis J, Cox-Foster D, Holmes EC, Briese T, Lipkin WI (2008) Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. J Virol 82:6209–6217CrossRefGoogle Scholar
  105. Paxton RJ, Klee J, Korpela S, Fries I (2007) Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38:558–565CrossRefGoogle Scholar
  106. Ratnieks FLW, Carreck NL (2010) Clarity on honey bee collapse? Science 327:152–153CrossRefGoogle Scholar
  107. Ribière M, Olivier V, Blanchard P (2010) Chronic bee paralysis: a disease and a virus like no other? J Invertebr Pathol 103:S120–S31CrossRefGoogle Scholar
  108. Richards AJ (2001) Does low biodiversity resulting from modern agriculture practice affect crop pollination and yield? Ann Bot 88:165–172CrossRefGoogle Scholar
  109. Ritter W, Leclercq E, Koch W (1984) Observation des populations d'abeilles et de Varroa dans les colonies à différents niveaux d'infestation. Apidologie 15:389–400CrossRefGoogle Scholar
  110. Roetschi A, Berthoud H, Kuhn R, Imdorf A (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 39:362–371CrossRefGoogle Scholar
  111. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119CrossRefGoogle Scholar
  112. Shimanuki H, Calderone NW, Knox DA (1994) Parasitic mite syndrome: the symptoms. Am Bee J 134:827–828Google Scholar
  113. Siede R, König M, Büchler R, Failing K, Thiel H-J (2008) A real-time PCR based survey on acute bee paralysis virus in German bee colonies. Apidologie 39:650–661CrossRefGoogle Scholar
  114. Solignac M, Vautrin D, Pizzo A, Navajas M, Le Conte Y, Cornuet JM (2003) Characterization of microsatellite markers from the apicultural pest Varroa destructor (Acari: Varroidae) and its relatives. Mol Ecol Notes 3:556–559CrossRefGoogle Scholar
  115. Solignac M, Cornuet J-M, Vautrin D, Le Conte Y, Anderson DL, Evans JD, Cros-Arteil S, Navajas M (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 272:411–419CrossRefGoogle Scholar
  116. Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends Ecol Evol 20:651–652CrossRefGoogle Scholar
  117. Sumner DA, Boriss H (2006) Bee-economics and the leap in pollination fees. ARE update. Giannini Found. Agric Econ 9:9–12Google Scholar
  118. Tapaszti Z, Forgách P, Kovágó C, Békési L, Bakonyi T, Rusvai M (2009) First detection and dominance of Nosema ceranae in Hungarian honeybee colonies. Acta Vet Hung 57:383–388CrossRefGoogle Scholar
  119. Tentcheva D, Gauthier L, Zappulla N, Dainat B, Cousserans F, Colin ME, Bergoin M (2004) Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol 70:7185–7191CrossRefGoogle Scholar
  120. Todd JH, De Miranda JR, Ball BV (2007) Incidence and molecular characterization of viruses found in dying New Zealand honey bee (Apis mellifera) colonies infested with Varroa destructor. Apidologie 38:354–367CrossRefGoogle Scholar
  121. Truper HG, dé Clari L (1998) Taxonomic note: erratum and correction of further specific epithets formed as sustantives (nouns) in apposition. Int J Syst Bacteriol 48:615CrossRefGoogle Scholar
  122. 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. J Invertebr Pathol 103:S80-S95CrossRefGoogle Scholar
  123. 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 147:599–603Google Scholar
  124. 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:e4071CrossRefGoogle Scholar
  125. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, Frazier M, Frazier J, Cox-Foster D, Chen Y, Underwood R, Tarpy DR, Pettis JS (2009) Colony collapse disorder: a descriptive study. PLoS One 4(8):e6481CrossRefGoogle Scholar
  126. Weber R, Bryan RT, Schwartz DA, Owen RL (1994) Human microsporidial infections. Clin Microbiol Rev 7:426–461Google Scholar
  127. White GF (1906) The bacteria of the apiary with special reference to bee disease. USDA, Bureau of Entomology, Technical Series 14:1–50Google Scholar
  128. White GF (1912) The cause of European foulbrood. US Department of Agriculture Bureau of Entomology Circular No. 157. US Department of Agriculture, WashingtonGoogle Scholar
  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 99–104Google Scholar
  130. Wilkins S, Brown M, Andrew A, Cuthbertson GS (2007) The incidence of honey bee pests and diseases in England and Wales. Pest Manag Sci 63:1062–1068CrossRefGoogle Scholar
  131. Williams GR, Shafer ABA, Rogers REL, Shutler D, Stewart DT (2008) First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and central USA. J Invertebr Pathol 97:189–192CrossRefGoogle Scholar
  132. Yang X, Cox-Foster DL (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 102:7470–7475CrossRefGoogle Scholar
  133. Yang X, Cox-Foster D (2007) Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology 134:405–412CrossRefGoogle Scholar
  134. Yue C, Genersch E (2005) RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J Gen Virol 86:3419–3424CrossRefGoogle Scholar
  135. Yue C, Schröder M, Bienefeld K, Genersch E (2006) Detection of viral sequences in semen of honeybees (Apis mellifera): evidence for vertical transmission of viruses through drones. J Invertebr Pathol 92:93–96CrossRefGoogle Scholar
  136. Yue C, Schröder M, Gisder S, Genersch E (2007) Vertical transmission routes for deformed wing virus of honeybees (Apis mellifera). J Gen Virol 88:2329–2336CrossRefGoogle Scholar
  137. Zander E (1909) Tierische Parasiten als Krankheitserreger bei der Biene. Münchener Bienenzeitung 31:196–204Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Institute for Bee ResearchHohen NeuendorfGermany

Personalised recommendations