, Volume 40, Issue 4, pp 419–428 | Cite as

Small hive beetle, Aethina tumida, as a potential biological vector of honeybee viruses

  • Michael Eyer
  • Yan Ping Chen
  • Marc Oliver Schäfer
  • Jeff Pettis
  • Peter NeumannEmail author
Original Article


The small hive beetle (SHB, Aethina tumida) is a parasite and scavenger of honeybee colonies. Here, we conducted laboratory experiments to investigate the potential of SHB as a vector of honeybee viruses. Using RT-PCR methods, Deformed Wing Virus (DWV) was detected in adult SHBs that: (1) were fed with dead workers with deformed wings, (2) were fed with DWV-positive brood, and (3) were associated with DWV-contaminated wax. SHB became significantly more often infected through feeding on virus infected workers, brood and the virus contaminated wax compared to pollen and the controls, where no infections were found. DWV was also detected in adult SHB after trophallaxis with infected workers. Further, among SHBs identified as DWV-positive, 40% of beetles carried negative stranded RNA of DWV, indicating virus replication. Our results suggest that SHB can be infected with honeybee viruses via food-borne transmission and have the potential of being a biological vector of honeybee viruses.

Apis mellifera Aethina tumida biological vector deformed wing virus honeybees small hive beetle 

Le Petit coléoptère des ruches, Aethina tumida, vecteur potentiel des virus de l’Abeille domestique

Apis mellifera Aethina tumida vecteur biologique virus de l’aile déformée DWV 

Der Kleine Beutenkäfer, Aethina tumida, ist ein potentieller Vektor von Viren der Honigbienen


Der Kleine Beutenkäfer, Aethina tumida (Coleoptera: Nitidulidae), ist ein Parasit von Völkern der Honigbiene, Apis mellifera, der sich als invasive Art rasch ausbreitet. Die Käfer paaren und vermehren sich innerhalb des Bienenstocks und können somit über verschiedene Kontaminierungswege mit Viren der Honigbiene infiziert werden. Wir präsentieren hier, mit Hilfe von RT-PCR Methoden, den ersten Nachweis von Honigbienenviren im Kleinen Beutenkäfer und in Bienenwachs. Der Kleine Beutenkäfer wurde in Käfigexperimenten mit dem Flügeldeformations-Virus (DWV) infiziert über: (1) Fütterung mit toten Arbeiterinnen mit klinischen Symptomen (deformierte Flügel), (2) Fütterung mit DWV positiver Bienenbrut, (3) Assoziation mit DWV kontaminiertem Wachs und (4) Trophallaxis mit infizierten Arbeiterinnen (Abb. 1). Wir fanden jedoch keinen Hinweis für eine orale Infektion über DWV kontaminierten Pollen (Abb. 1). In 40 % der DWV positiven Käferproben konnte der minus RNA Strang des DWV nachgewiesen werden (Abb. 2), was ein Hinweis dafür ist, dass sich das +RNA Virus im Käfer vermehren kann. Unsere Ergebnisse zeigen zum ersten Mal, dass eine orale Infektion mit Honigbienenviren über Wachs möglich ist. Darüber hinaus ist der Kleine Beutenkäfer ein potentieller biologischer Vektor von Honigbienenviren, was für deren Verbreitung innerhalb und zwischen Völkern relevant sein kann.

Apis mellifera Aethina tumida biologischer Vektor Deformed Wing Virus Honigbiene Kleiner Beutenkäfer 


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  1. Anderson D.L. (1991) Kashmir bee virus-a relatively harmless virus of honey bee colonies, Am. Bee J. 131, 767–770.Google Scholar
  2. Allen M., Ball B.V. (1996) The incidence and world distribution of honeybee viruses, Bee World 77, 141–162.Google Scholar
  3. Bailey L. (1969) The multiplication and spread of sac brood virus of bees, Ann. Appl. Biol. 63, 483–491.PubMedCrossRefGoogle Scholar
  4. Bailey L. (1976) Viruses attacking the honey bee, Adv. Virus Res. 20, 271–304.PubMedCrossRefGoogle Scholar
  5. Bailey L., Ball B.V. (1991) Honey bee pathology, 2nd ed., Academic Press, London, United Kingdom.Google Scholar
  6. Bakonyi T., Farkas R., Szendroi A., Dobos-Kovacs M., Rusvai M. (2002) Detection of acute bee paralysis virus by RT-PCR in honey bee and Varroa destructor field samples: rapid screening of representative Hungarian apiaries, Apidologie 33, 63–74.CrossRefGoogle Scholar
  7. Bowen-Walker P.L., Martin S.J., 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, 101–106.PubMedCrossRefGoogle Scholar
  8. Buchholz S., Schäfer M.O., Spiewok S., Pettis J.S., Duncan M., Ritter W., Spooner-Hart R., Neumann P. (2008) Alternative food sources of Aethina tumida (Coleoptera: Nitidulidae), J. Apic. Res. 47, 201–208.Google Scholar
  9. Celle O., Blanchard P., Olivier V., Schurr F., Cougoule N., Faucon J.-P., Ribière M. (2008) Detection of Chronic bee paralysis virus (CBPV) genome and its replicative RNA form in various hosts and possible ways of spread, Virus Res. 133, 280–284.PubMedCrossRefGoogle Scholar
  10. Chen Y.P., Siede R. (2007) Honeybee viruses, Adv. Virus Res. 70, 33–80.PubMedCrossRefGoogle Scholar
  11. Chen Y.P., Higgins J.A., Feldlaufer M.F. (2005) Quantitative Real-Time Reverse TranscriptionPCR Analysis of Deformed Wing Virus Infection in the Honeybee (Apis mellifera L.), Appl. Environ. Microbiol. 71, 436–441.PubMedCrossRefGoogle Scholar
  12. Chen Y.P., Evans J.D., Feldlaufer M.F. (2006a) Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera, J. Invertebr. Pathol. 92, 152–159.PubMedCrossRefGoogle Scholar
  13. Chen Y.P., Pettis J.S., Collins A., Feldlaufer M.F. (2006b) Prevalence and transmission of honey bee viruses, Appl. Environ. Microbiol. 72, 606–611.PubMedCrossRefGoogle Scholar
  14. Cox-Foster D.L., Conlan S., Holmes E.C., Palacios G., Evans J.D., Moran N.A., Quan P.-L., Briese T., Hornig M., Geiser D.M., Martinson V., van Engelsdorp D., Kalkstein A.L., Drysdale A., Hui J., Zhai J., Cui L., Hutchison S.K., Simons J.F., Egholm M., Pettis J.S., Lipkin W.I. (2007) A Metagenomic Survey of Microbes in Honey Bee Colony Collapse Disorder, Science 318, 283–287.PubMedCrossRefGoogle Scholar
  15. Dainat B., Ken T., Berthoud H., Neumann P. (2008) The ectoparasitic mite Tropilaelaps mercedesae (Acari: Laelapidae) as a vector of honeybee viruses, Insectes Soc., DOI 10.1007/s00040-008-1030-5.Google Scholar
  16. Domingo E., Holland J.J. (1997) RNA virus mutations and fitness for survival, Annu. Rev. Microbiol. 51, 151–178.PubMedCrossRefGoogle Scholar
  17. Domingo E., Baranowski E., Ruiz-Jarabo C.M., Martín-Hernández A.M., Sáiz J.C., Escarmís C. (1998) Quasispecies Structure and Persistence of RNA Viruses, Emerg. Infect. Dis. 4, 521–527.PubMedCrossRefGoogle Scholar
  18. Ellis J.D., Neumann P., Hepburn H.R., Elzen P.J. (2002a) Longevity and reproductive success of Aethina tumida (Coleoptera: Nitidulidae) fed different natural diets, J. Econ. Entomol. 95, 902–907.PubMedCrossRefGoogle Scholar
  19. Ellis J.D., Pirk C.W.W., Hepburn H.R., Kastberger G., Elzen P.J. (2002b) Small hive beetles survive in honeybee prisons by behavioural mimicry, Naturwissenschaften 89, 326–328.PubMedCrossRefGoogle Scholar
  20. Elzen P.J., Baxter J.R., Westervelt D., Randall C., Wilson W.T. (2000) A scientific note on observations of the small hive beetle, Aethina tumida Murray (Coleoptera, Nitidulidae), in Florida, USA, Apidologie 31, 593–594.CrossRefGoogle Scholar
  21. Elzen P.J., Baxter J.R., Neumann P., Solbrig A.J., Pirk C.W.W., Hepburn H.R., Westervelt D., Randall C. (2001) Behavior of African and European subspecies of Apis mellifera toward the small hive beetle, Aethina tumida, J. Apic. Res. 40, 40–41.Google Scholar
  22. Genbank database at the National Center for Biotechnology, NC_004830 and AY292384 [online] (accessed on 15 September 2008).Google Scholar
  23. Genersch E., Yue C., Fries I., de Miranda J.R. (2006) Detection of deformed wing virus, a honey bee viral pathogen, in bumble bee (Bombus terrestris and Bombus pascuorum) with wing deformities, J. Invertebr. Pathol. 91, 61–63.PubMedCrossRefGoogle Scholar
  24. Hoffmann D., Pettis J.S., Neumann P. (2008) Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens), Insectes Soc. 55, 153–162.CrossRefGoogle Scholar
  25. Holland J., Spindler K., Horodyski F., Grabau E., Nichol S., Vandepol S. (1982) Rapid evolution of RNA genomes, Science 215, 1577–1585.PubMedCrossRefGoogle Scholar
  26. Lanzi G., de Miranda J.R., Boniotti M.B., Cameron C.E., Lavazza A., Capucci L., Camazine S.M., Rossi C. (2006) Molecular and biological characterization of deformed wing virus of honey bees (Apis mellifera), J. Virol. 80, 4998–5009.PubMedCrossRefGoogle Scholar
  27. Lundie A.E. (1940) The small hive beetle Aethina tumida, Science Bulletin 220, Dep. Agr. Forestry, Government Printer, Pretoria, South Africa.Google Scholar
  28. Martin S.J. (2001) The role of Va r r o a and viral pathogens in the collapse of honeybee colonies: a modeling approach, J. Appl. Ecol. 38, 1082–1093.CrossRefGoogle Scholar
  29. Morse R.A. (1972) The complete guide to beekeeping, E. P. & Co. Dutton, New YorkGoogle Scholar
  30. Mürrle T.M., Neumann P. (2004) Mass production of small hive beetles (Aethina tumida Murray, Coleoptera: Nitidulidae), J. Apic. Res. 43, 144–145.Google Scholar
  31. Neumann P., Elzen P.J. (2004) The biology of the small hive beetle (Aethina tumida, Coleoptera: Nitidulidae): gaps in our knowledge of an invasive species, Apidologie 35, 229–247.CrossRefGoogle Scholar
  32. Neumann P., Ellis J.D. (2008) The small hive beetle (Aethina tumida Murray, Coleoptera: Nitidulidae): distribution, biology and control of an invasive species, J. Apic. Res. 47, 180–183.CrossRefGoogle Scholar
  33. Neumann P., Pirk C.W.W., Hepburn H.R., Solbrig A.J., Ratnieks F.L.W., Elzen P.J., Baxter J.R. (2001a) Social encapsulation of beetle parasites by Cape honeybee colonies (Apis mellifera capensis Esch.), Naturwissenschaften 88, 214–216.PubMedCrossRefGoogle Scholar
  34. Neumann P., Pirk C.W.W., Hepburn H.R., Elzen P.J., Baxter J.R. (2001b) Laboratory rearing of small hive beetles (Aethina tumida), J. Apic. Res. 40, 111–112.Google Scholar
  35. Ongus J.R., Peters D., Bonmatin J.-M., Bengsch E., Vlak J.M., Van Oers M.M. (2004) Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor, J. Gen. Virol. 85, 3747–3755.PubMedCrossRefGoogle Scholar
  36. Ribière M., Lallemand P., Iscache A.L., Schurr F., Celle O., Blanchard P., Olivier V., Faucon J.P. (2007) Spread of infectious Chronic bee paralysis virus by honeybee (Apis mellifera L.) faeces, Appl. Environ. Microbiol. 73, 7711–7716.PubMedCrossRefGoogle Scholar
  37. Schäfer M.O., Pettis J.S., Ritter W., Neumann P. (2008) A scientific note on quantitative diagnosis of small hive beetles, Aethina tumida, in the field, Apidologie 39, 564–565.CrossRefGoogle Scholar
  38. Shen M.Q., Cui L.W., Ostiguy N., Cox-Foster D. (2005) 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. 86, 2281–2289.PubMedCrossRefGoogle Scholar
  39. Spiewok S., Pettis J.S., Duncan M., Spooner-Hart R., Westervelt D., Neumann P. (2007) Small hive beetle, Aethina tumida, populations I: Infestation levels of honeybee colonies, apiaries and regions, Apidologie 38, 595–605.CrossRefGoogle Scholar
  40. Spiewok S., Duncan M., Spooner-Hart R., Pettis J.S., Neumann P. (2008) Small hive beetle, Aethina tumida, populations II: Dispersal of small hive beetles, Apidologie 39, 683–693.CrossRefGoogle Scholar
  41. Schmolke M.D. (1974) A study of Aethina tumida: the small hive beetle, Project Report, University of Rhodesia.Google Scholar
  42. Tentcheva D., Gauthier L., Jouve S., Canabady-Rochelle L., Dainat B., Cousserans F., Colin M.E., Ball B.V., Bergoin M. (2004a) Polymerase Chain Reaction detection of deformed wing virus (DWV) in Apis mellifera and Varroa destructor, Apidologie 35, 431–439.CrossRefGoogle Scholar
  43. Tentcheva D., Gauthier L., Zappulla N., Dainat B., Cousserans F., Colin M.E., Bergoin M. (2004b) 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.PubMedCrossRefGoogle Scholar
  44. Tentcheva D., Gauthier L., Bagny L., Fievet J., Dainat B., Cousserans F., Colin M.E., Bergoin M. (2006) Comparative analysis of deformed wing virus (DWV) RNA in Apis mellifera and Varroa destructor, Apidologie 37, 41–50.CrossRefGoogle Scholar
  45. Voinnet O. (2001) RNA silencing as a plant immune system against viruses, Trends Genet. 17, 449–459.PubMedCrossRefGoogle Scholar
  46. Vignuzzi M., Stone J.K., Arnold J.J., Cameron C.E., Andino R. (2006) Quasispecies diversity determines pathogenesis through cooperative interactions within a viral population, Nature 439, 344–348.PubMedCrossRefGoogle Scholar
  47. Yen Y., Green P.J. (1991) Identification and properties of the major ribonucleases of Arabidopsis thaliana, Plant Physiol. 97, 1487–1493.PubMedCrossRefGoogle Scholar
  48. Yue C., Genersch E. (2005) RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor), J. Gen. Virol. 86, 3419–3424.PubMedCrossRefGoogle Scholar
  49. Woolhouse M.E.J., Taylor L.H., Haydon D.T. (2001) Population biology of multihost pathogens, Science 292 (5519), 1109–1112.PubMedCrossRefGoogle Scholar

Copyright information

© Springer S+B Media B.V. 2009

Authors and Affiliations

  • Michael Eyer
    • 1
  • Yan Ping Chen
    • 2
  • Marc Oliver Schäfer
    • 1
    • 3
  • Jeff Pettis
    • 2
  • Peter Neumann
    • 1
    • 4
    • 5
    Email author
  1. 1.Swiss Bee Research CentreAgroscope Liebefeld-Posieux Research Station ALPBernSwitzerland
  2. 2.USDA-ARS Bee Research LaboratoryBeltsvilleUSA
  3. 3.Chemisches und Veterinäruntersuchungsamt Freiburg (CVUA), Fachgebiet BienenFreiburgGermany
  4. 4.Eastern Bee Research Institute of Yunnan Agricultural UniversityKunmingChina
  5. 5.Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa

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