Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata)

Journal of Invertebrate Pathology

Volumn 114, Issue 1, 2013, Pages 45-52

  Strauss, Ursula ^a   Human, Hannelie ^a   Gauthier, Laurent ^a   Crewe, Robin M ^a   Dietemann, Vincent ^a,b   Pirk, Christian W W ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b AGROSCOPE LIEBEFELD POSIEUX RESEARCH STATION ALP   (Switzerland)

Author keywords

Apis mellifera scutellata; Honeybee; Parasite; Pathogen; Varroa destructor; Virus

Indexed keywords

ANIMAL; APIS MELLIFERA SCUTELLATA; ARTICLE; BEE; COMPARATIVE STUDY; GENETICS; HONEYBEE; ISOLATION AND PURIFICATION; MICROBIOLOGY; NOSEMA; PARASITE; PARASITOLOGY; PATHOGENESIS; PREVALENCE; SEASON; SOUTH AFRICA; VARROA DESTRUCTOR; VARROIDAE; VIROLOGY; VIRUS;

APIS MELLIFERA SCUTELLATA; HONEYBEE; PARASITE; PATHOGEN; VARROA DESTRUCTOR; VIRUS;

ANIMALS; BEES; NOSEMA; PREVALENCE; SEASONS; SOUTH AFRICA; VARROIDAE;

EID: 84880839110     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2013.05.003     Document Type: Article

References (103)

1. Allen M.F., Ball B.V. The incidence and world distribution of the honey bee viruses. Bee World 1996, 77:141-162.
2. Allsopp M. Varroa jacobsoni in South Africa. S. Afr. Bee J. 1997, 69:73-82.
3. Allsopp M. Cape honeybee (Apis mellifera capensis Eshscholtz) and Varroa mite (Varroa destructor Anderson & Trueman) threats to honeybees and beekeeping in Africa. Int. J. Trop. Insect Sci. 2004, 24:87-94.
4. Allsopp, M., 2006. Analysis of Varroa destructor Infestation of Southern African Honey Bee Populations. M.Sc. Thesis. University of Pretoria, Pretoria, South Africa.
5. Allsopp M., Crewe R.M. The Cape honeybee as a Trojan horse rather than the hordes of Jenghiz Khan. Am. Bee J. 1993, 133:121-123.
6. Bailey L., Ball B.V. Honey Bee Pathology 1991, Academic Press, London.
7. Bailey L., Ball B.V., Perry J.N. Association of viruses with two protozoan pathogens of the honey bee. Ann. Appl. Biol. 1983, 103:13-20.
8. Baker A., Schroeder D. Occurrence and genetic analysis of picorna-like viruses infecting worker bees of Apis mellifera L. populations in Devon, South West England. J. Invertebr. Pathol. 2008, 98:239-242.
9. Ball, B.V., 1989. Varroa jacobsoni as a virus vector. In: Cavalloro, R. (Ed.), Present Status of Varroatosis in Europe and Progress in the Varroa mite Control. Proceedings of a Meeting of the EC Expert Group, Luxembourg, pp. 241-244.
10. Ball B.V., Allen M.F. The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni. Ann. Appl. Biol. 1988, 113:237-244.
11. Baxter A. American foulbrood (AFB) in the Western Cape: advisory notice. S. Afr. Bee J. 2009, 81:8-9.
12. Belloy L., Imdorf A., Fries I., Forsgren E., Berthoud H., Kuhn R., Charrière J.D. Spatial distribution of Melissococcus plutonius in adult honeybees collected from apiaries and colonies with and without symptoms of European foulbrood. Apidologie 2007, 38:136-140.
13. Berényi O., Bakonyi T., Derakhshifar I., Koglberger H., Nowotny N. Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl. Environ. Microbiol. 2006, 72:2414-2420.
14. Berthoud H., Imdorf A., Haueter M., Radloff S., Neumann P. Virus infections and winter losses of honey bee colonies (Apis mellifera). J. Apicult. Res. 2010, 49:60-65.
15. Bowen-Walker P.L., Martin S.J., Gunn A. The transmission of deformed wing virus between honey bees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J. Invertebr. Pathol. 1999, 73:101-106.
16. Brodschneider R., Moosbeckhofer R., Crailsheim K. Surveys as a tool to record winter losses of honey bee colonies: a two year case study in Austria and South Tyrol. J. Apicult. Res. 2010, 49:23-30.
17. Buys, B., 1976. Nosema incidence of honeybee on the Cape breeding station. In: Fletcher, D.J.C. (Ed.), African Bees: Taxonomy, Biology and Economic Use. Apimondia International Symposium, Pretoria, pp. 84-90.
18. Buys B. A survey on honeybee pests in South Africa. S. Afr. Bee J. 1982, 54:86-90.
19. Calderón R.A., Van Veen J., Arce H.G., Esquivel M.E. Presence of deformed wing virus and Kashmir bee virus in Africanized honey bee colonies in Costa Rica infested with Varroa destructor. Bee World 2003, 84:112-116.
20. Camazine S., Morse R.A. The Africanized honeybee: the epithet "killer bee" is undeserved. Am. Sci. 1988, 76:464-471.
21. Carreck N.L., Ball B.V., Wilson J.K. Virus succession in honey bee colonies infested with Varroa destructor. Apiacta 2002, 37:44-48.
22. Chantawannakul P., Ward L., Boonham N., Brown M. A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honeybee (Apis mellifera) apiary. J. Invertebr. Pathol. 2006, 91:69-73.
23. Chen Y.P., Pettis J.S., Collins A., Feldlaufer M.F. Prevalence and transmission of honeybee viruses. Appl. Environ. Microbiol. 2006, 72:606-611.
24. Chen Y.P., Siede R. Honey bee viruses. Adv. Virus Res. 2007, 70:33-80.
25. Crane A. Bees and Beekeeping, Science, Practice and World Resources 1990, Heinemann Professional Publishing Ltd., Halley Court, Jordan Hills, Oxford.
26. Dainat B., Evans J.D., Chen Y.P., Gauthier L., Neumann P. Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Appl. Environ. Microbiol. 2012, 78:981-987.
27. Dainat B., Evans J.D., Chen Y.P., Gauthier L., Neumann P. Predictive markers of honey bee colony collapse. PLoS One 2012, 7:e32151.
28. Davison S., Govan V., Leat N., Allsopp M. Bee diseases in South Africa 1: EFB, AFB, chalkbrood and bee viruses. S. Afr. Bee J. 1999, 71:84-87.
29. Di Prisco G., Pennacchio F., Caprio E., Boncristiani H.F., Evans J.D., Chen Y.P. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J. Gen. Virol. 2011, 92:151-155.
30. Dietemann V., Lubbe A., Crewe R.M. Human factors facilitating the spread of a parasitic honey bee in South Africa. J. Econ. Entomol. 2006, 99:7-13.
31. Dietemann V., Pflugfelder J., Anderson D., Charrière J.D., Chejanovsky N., Dainat B., de Miranda J.R., Delaplane K., Dillier F.X., Fuchs S., Gallmann P., Gauthier L., Imdorf A., Koeniger N., Kralj J., Meikle W., Pettis J., Rosenkranz P., Sammataro D., Smith D., Yañez O., Neumann P. Varroa destructor: research avenues towards sustainable control. J. Apicult. Res. 2012, 51:125-132.
32. Dietemann V., Pirk C.W.W., Crewe R.M. Is there a need for conservation of honeybees in Africa?. Apidologie 2009, 40:285-295.
33. Ellis J.D., Munn P.A. The worldwide health status of honey bees. Bee World 2005, 86:88-101.
34. Fletcher D.J.C. The African bee, Apis mellifera adansonii, in Africa. Annu. Rev. Entomol. 1978, 23:151-171.
35. Forgach P., Bakonyi T., Tapaszti Z., Nowotny N., Rusvai M. Prevalence of pathogenic bee viruses in Hungarian apiaries: situation before joining the European Union. J. Invertebr. Pathol. 2008, 98:235-238.
36. Francis R.M., Kryger P. Single assay detection of acute bee paralysis virus, Kashmir bee virus and Israeli acute paralysis virus. J. Apicult. Sci. 2012, 56:137-145.
37. Fries I. Nosema ceranae in European honey bees (Apis melllifera). J. Invertebr. Pathol. 2010, 103:S73-S79.
38. Gauthier L., Ravallec M., Tournaire M., Cousserans F., Bergoin M., Dainat B., de Miranda J.R. Viruses associated with ovarian degeneration in Apis mellifera L. queens. PLoS One 2011, 6:e16217.
39. Genersch E. Honey bee pathology: current threats to honey bees and beekeeping. Appl. Microbiol. Biotechnol. 2010, 87:87-97.
40. Genersch E., Von Der Ohe W., Kaatz H., Schroeder A., Otten C., Büchler R., Berg S., Ritter W., Muhlen W., Gisder S., Meixner M., Liebig G., Rosenkranz P. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 2010, 41:332-352.
41. Gidey A., Mulugeta S., Fromsa A. Prevalence of bee lice Braula coeca (Diptera: Braulidae) and other perceived constraints to honey bee production in Wukro Woreda, Tigray Region Ethiopia. Global Vet. 2012, 8:631-635.
42. Gisder S., Aumeier P., Genersch E. Deformed wing virus (DWV): viral load and replication in mites (Varroa destructor). J. Gen. Virol. 2009, 90:463-467.
43. Guzman-Novoa E., Eccles L., Calvete Y., McGowan J., Kelly P.G., Correa-Benitez A. Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie 2010, 41:443-450.
44. Härtel S., Neumann P., Kryger P., von der Heide C., Moltzer G.J., Crewe R.M., van Praagh J.P., Moritz R.F.A. Infestation levels of Apis mellifera scutellata swarms by socially parasitic Cape honeybee workers (Apis mellifera capensis). Apidologie 2006, 37:462-470.
45. Hepburn H.R. The bee louse. S. Afr. Bee J. 1978, 50:11-12.
46. Hepburn H.R., Radloff S.E. Honeybees of Africa 1998, Springer, Berlin.
47. Higes M., Martín-Hernández R., Garrido-Bailon E., Botias C., Meana A. The presence of Nosema ceranae (Microsporidia) in North African honey bees (Apis mellifera intermissa). J. Apicult. Res. 2009, 48:217-219.
48. Higes M., Martín-Hernández R., Garrido-Bailón E., Botías C., García-Palencia P., Meana A. Regurgitated pellets of Merops apiaster as fomites of infective Nosema ceranae (Microsporidia) spores. Environ. Microbiol. 2008, 5:1374-1379.
49. Human H., Pirk C.W.W., Crewe R.M., Dietemann V. The honeybee disease American foulbrood - an African perspective. Afr. Entomol. 2011, 19:551-557.
50. Jaffé R., Dietemann V., Allsopp M., Costa C., Crewe R.M., Dall'Olio R., De La Rúa P., El-Niweiri M.A.A., Fries I., Kezic N., Meusel M.S., Paxton R.J., Shaibi T., Stolle E., Moritz R.F.A. Estimating the density of honey bee colonies across their natural range to fill the gap in pollinator decline censuses. Conserv. Biol. 2009, 24:583-593.
51. Johns, J., 2003. Investigation into South African Honey Bee Viruses and their Association with the Parasitic mite Varroa destructor (Acarini: Varroidae). M.Sc. Thesis. University of the Western Cape, Cape Town, South Africa.
52. Kajobe R., Marris G., Budge G., Laurenson L., Cordoni G., Jones B., Wilkins S., Cuthbertson A.G.S., Brown M.A. First molecular detection of a viral pathogen in Ugandan honey bees. J. Invertebr. Pathol. 2010, 104:153-156.
53. Kraus F.B., Franck P., Vandame R. Asymmetric introgression of African genes in honeybee populations (Apis mellifera L.) in Central Mexico. Heredity 2007, 99:233-240.
54. Kryger P., Dietemann V., Crewe R.M. Have we found a solution to the Capensis problem?. S. Afr. Bee J. 2003, 75:123-128.
55. Leat N., Ball B., Govan V., Davison S. Analysis of the complete genome sequence of black queen-cell virus, a picorna-like virus of honey bees. J. Gen. Virol. 2000, 81:2111-2119.
56. Le Conte Y., Ellis M., Ritter W. Varroa mites and honey bee health: can Varroa explain part of the colony losses?. Apidologie 2010, 41:353-363.
57. Liu T. Varroa mites as carriers of honey bee chalkbrood. Am. Bee J. 1996, 136:655.
58. Locke B., Forsgren E., Fries I., de Miranda J.R. Acaricide treatment affects viral dynamics in Varroa destructor-infested honey bee colonies via both host physiology and mite control. Appl. Environ. Microbiol. 2012, 78:227-235.
59. Lundie, A.E., 1940. The Small Hive Beetle: Aethina tumida. Science Bulletin 220. Union of South Africa. Department of Agriculture and Forestry Entomological Series 3.
60. Maori E., Lavi S., Mozes-Koch R., Gantman Y., Peretz Y., Edelbaum O., Tanne E., Sela I. Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra-and inter-species recombination. J. Gen. Virol. 2007, 88:3428-3438.
61. Martin S.J. The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J. Appl. Ecol. 2001, 38:1082-1093.
62. Martin S.J., Kryger P. Reproduction of Varroa destructor in South African honey bees: does cell space influence Varroa male survivorship?. Apidologie 2002, 33:51-61.
63. Martin S.J., Highfield A.C., Brettell L., Villalobos E.M., Budge G.E., Powell M., Nikaido S., Schroeder D.C. Global honey bee viral landscape altered by a parasitic mite. Science 2012, 336:1304-1306.
64. Martin S.J., Hogarth A., Van Breda J., Perrett J. A scientific note on Varroa jacobsoni Oudemans and the collapse of Apis mellifera colonies in the United Kingdom. Apidologie 1998, 29:369-370.
65. Medina L.M., Mejia E.V. The presence of Varroa jacobsoni mite and Ascosphaera apis fungi in collapsing and normal honey bee (Apis mellifera L.) colonies in Yucatan, Mexico. Am. Bee J. 1999, 139:794-796.
66. Moritz R.F.A., Härtel S., Neumann P. Global invasions of the western honey bee (Apis mellifera) and the consequences for biodiversity. Ecoscience 2005, 12:289-301.
67. Moritz R.F.A., Pirk C.W.W., Hepburn H.R., Neumann P. Short-sighted evolution of virulence in parasitic honeybee workers (Apis mellifera capensis Esch.). Naturwissenschaften 2008, 95:507-513.
68. Morse R.A., Calderone N.W. The value of honey bee pollination in the United States. Bee Cult. 2000, 128:1-15.
69. Nazzi F., Brown S.P., Annoscia D., Del Piccolo F., Di Prisco G., Varricchio P., Della Vedova G., Cattonaro F., Caprio E., Pennacchio F. Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathogens 2012, 8:e1002735.
70. Neumann P., Carreck N.L. Honey bee colony losses. J. Apicult. Res. 2010, 49:1-6.
71. Neumann P., Moritz R.F.A. The Cape honeybee phenomenon: the sympatric evolution of a social parasite in real time?. Behav. Ecol. Sociobiol. 2002, 52:271-281.
72. Neumann P., Radloff S.E., Moritz R.F.A., Hepburn H.R., Reece S.L. Social parasitism by honeybee workers (Apis mellifera capensis Esch.): host finding and resistance of hybrid host colonies. Behav. Ecol. 2001, 12:419-428.
73. OIE Report, 2009. American Foulbrood of Honeybees, South Africa. OIE Reference: 1092. (13.03.13). http://www.oie.int/wahis_2/public.
74. Ongus, J.R., 2006. Varroa destructor Virus 1: A New Picorna-like Virus in Varroa mites as Well as Honey Bees. Ph.D. Thesis. Wageningen University, The Netherlands.
75. Ostiguy S. Sustainable beekeeping: managed pollinator CAP coordinated agricultural project - a national research and extension initiative to reverse pollinator decline. Am. Bee J. 2010, 150:149-152.
76. Palacios G., Hui J., Quan P.L., Kalkstein A., Honkavuori K.S., Bussetti A.V., Conlan S., Evans J., Chen Y.P., vanEngelsdorp D., Efrat H., Pettis J., Cox-Foster D., Holmes E.C., Briese T., Lipkin W.I. Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. J. Virol. 2008, 82:6209-6217.
77. Ribière M., Ball B.V., Aubert M.F.A. Natural history and geographic distribution of honey bee viruses. Virology and the Honey Bee, VIth Framework 2008, 15-84. EC Publications, Brussels. M.F.A. Aubert, B.V. Ball, I. Fries, N. Milani, R.F.A. Moritz (Eds.).
78. Ribière M., Olivier V., Blanchard P. Chronic bee paralysis: a disease and a virus like no other?. J. Invertebr. Pathol. 2010, 103:120-131.
79. Ritter W. Varroa disease of the honeybee Apis mellifera. Bee World 1981, 62:141-153.
80. Roetschi A., Berthoud H., Kuhn R., Imdorf A. 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 2008, 39:362-371.
81. Rosenkranz P., Aumeier P., Ziegelmann B. Biology and control of Varroa destructor. J. Invertebr. Pathol. 2010, 103:96-119.
82. Sammataro D., Gerson U., Needham G. Parasitic mites of honey bees: life history, implications, and impact. Annu. Rev. Entomol. 2000, 45:519-548.
83. Schäfer M.O., Ritter W., Pettis J.S., Neumann P. Winter losses of honeybee colonies (Hymenoptera: Apidae): the role of infestations with Aethina tumida (Coleoptera: Nitidulidae) and Varroa destructor (Parasitiformes: Varroidae). J. Econ. Entomol. 2010, 103:10-16.
84. Schneider S.S., DeGrandi-Hoffman G., Smith D.R. The African honey bee: factors contributing to a successful biological invasion. Annu. Rev. Entomol. 2004, 49:351-376.
85. Shen M., Cui L., Ostiguy N., Cox-Foster D. Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic Varroa mite. J. Gen. Virol. 2005, 86:2281-2289.
86. Shimanuki H., Calderone N.W., Knox D.A. Parasitic mite syndrome: the symptoms. Am. Bee J. 1994, 134:827-828.
87. Stokstad E. The case of the empty hives. Science 2007, 316:970-972.
88. Sumpter D.J.T., Martin S.J. The dynamics of virus epidemics in Varroa infested honey bee colonies. J. Anim. Ecol. 2004, 73:51-63.
89. Swart, D.J., 2001. Specialized management. In: Johannsmeier, M.F. (Ed.), Beekeeping in South Africa. Plant Protection Handbook No. 14. Agricultural Research Council, Pretoria, pp. 85-94.
90. Swart, D.J., 2003. The Occurrence of Nosema apis (Zander), Acarapis woodi (Rennie), and the Cape Problem Bee in the Summer Rainfall Region of South Africa. M.Sc. Thesis. Rhodes University, Grahamstown, South Africa.
91. Swart, D.J., Johannsmeier, M.R., Tribe, G.D., Kryger, P., 2001. Diseases and pests of honeybees. In: Johannsmeier, M.F. (Ed.), Beekeeping in South Africa. Plant Protection Handbook No. 14. Agricultural Research Council, Pretoria, pp. 198-222.
92. Teixeira E.W., Chen Y.P., Message D., Pettis J., Evans J.D. Virus infections in Brazilian honey bees. J. Invertebr. Pathol. 2008, 99:117-119.
93. Tentcheva D., Gauthier L., Zappulla N., Dainat B., Cousserans F., Colin M.E., Bergoin M. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl. Environ. Microbiol. 2004, 70:7185-7191.
94. Valera F., Martín-Hernández R., Higes M. Evaluation of large-scale dissemination of Nosema ceranae spores by European bee-eaters Merops apiaster. Environ. Microbiol. Rep. 2011, 3:47-53.
95. vanEngelsdorp D., Hayes J., Underwood R.M., Pettis J.S. A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS One 2008, 3:e4071.
96. vanEngelsdorp D., Hayes J., Underwood R.M., Pettis J.S. A survey of honey bee colony losses in the United States, fall 2008 to spring 2009. J. Apicult. Res. 2010, 49:7-14.
97. Welch A., Drummond F., Tewari S., Averill A., Burand J.P. Presence and prevalence of viruses in local and migratory honeybees (Apis mellifera) in Massachusetts. Appl. Environ. Microbiol. 2009, 75:7862-7865.
98. Wilson W.T. Resistance to American foulbrood in honey bees. XI. Fate of Bacillus larvae spores ingested by adults. J. Invertebr. Pathol. 1971, 17:247-255.
99. Yañez O., Jaffé R., Jarosch A., Fries I., Moritz R.F.A., Paxton R.J., de Miranda J.R. Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): implications for sexual transmission of a major honey bee virus. Apidologie 2012, 43:17-30.
100. Yang X., Cox-Foster D. Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc. Natl. Acad. Sci. USA 2005, 102:7470-7475.
101. Yue C., Genersch E. RT-PCR analysis of deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J. Gen. Virol. 2005, 86:3419-3424.
102. Zaitoun S., Al-Ghzawi A.A. Daily number of bee louse (Braula coeca) in honey bee (Apis mellifera carnica and A. m. syriaca) colonies maintained under semi-arid conditions. Insect Sci. 2008, 15:563-567.
103. Zioni N., Soroker V., Chejanovsky N. Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1 - deformed wing virus recombinant (VDV-1-DWV) in the head of the honey bee. Virology 2011, 417:106-112.