Skip to main content
SpringerLink
Log in

Infestation of Japanese Native Honey Bees by Tracheal Mite and Virus from Non-native European Honey Bees in Japan

  • Invertebrate Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Invasion of alien species has been shown to cause detrimental effects on habitats of native species. Insect pollinators represent such examples; the introduction of commercial bumble bee species for crop pollination has resulted in competition for an ecological niche with native species, genetic disturbance caused by mating with native species, and pathogen spillover to native species. The European honey bee, Apis mellifera, was first introduced into Japan for apiculture in 1877, and queen bees have been imported from several countries for many years. However, its effects on Japanese native honey bee, Apis cerana japonica, have never been addressed. We thus conducted the survey of honey bee viruses and Acarapis mites using both A. mellifera and A. c. japonica colonies to examine their infestation in native and non-native honey bee species in Japan. Honey bee viruses, Deformed wing virus (DWV), Black queen cell virus (BQCV), Israeli acute paralysis virus (IAPV), and Sacbrood virus (SBV), were found in both A. mellifera and A. c. japonica colonies; however, the infection frequency of viruses in A. c. japonica was lower than that in A. mellifera colonies. Based on the phylogenies of DWV, BQCV, and SBV isolates from A. mellifera and A. c. japonica, DWV and BQCV may infect both honey bee species; meanwhile, SBV has a clear species barrier. For the first time in Japan, tracheal mite (Acarapis woodi) was specifically found in the dead honey bees from collapsing A. c. japonica colonies. This paper thus provides further evidence that tracheal-mite-infested honey bee colonies can die during cool winters with no other disease present. These results demonstrate the infestation of native honey bees by parasite and pathogens of non-native honey bees that are traded globally.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Altizer S, Harvell D, Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evol 18:589–596

    Article  Google Scholar 

  2. Bailey L, Ball BV (1978) Apis iridescent virus and "clustering disease" of Apis cerana. J Invertebr Pathol 31:368–371

    Article  CAS  PubMed  Google Scholar 

  3. Bailey L, Carpenter JM, Woods RD (1982) A strain of Sacbrood virus from Apis cerana. J Invertebr Pathol 39:264–265

    Article  Google Scholar 

  4. Bakonyi T, Grabensteiner E, Kolodziejek J, Rusvai M, Topolska G, Ritter W, Nowotny N (2002) Phylogenetic analysis of acute bee paralysis virus strains. Appl Environ Microbiol 68:6446–6450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Benjeddou M, Leat N, Allsopp M, Davison S (2001) Detection of acute bee paralysis virus and black queen cell virus from honeybees by reverse transcriptase PCR. Appl Environ Microbiol 67:2384–2387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Berényi O, Bakonyi T, Derakhshifar I, Köglberger H, Topolska G, Ritter W, Pechhacker H, Nowotny N (2007) Phylogenetic analysis of deformed wing virus genotypes from diverse geographic origins indicates recent global distribution of the virus. Appl Environ Microbiol 73:3605–3611

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chen YP, Siede R (2007) Honey bee viruses. Adv Virus Res 70:33–80

    Article  CAS  PubMed  Google Scholar 

  8. Chen Y, Evans JD, Zhou L, Boncristiani H, Kimura K, Xiao T, Litkowski AM, Pettis JS (2009) Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J Invertebr Pathol 101:204–209

    Article  PubMed  Google Scholar 

  9. Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol Conserv 129:461–467

    Article  Google Scholar 

  10. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  11. Delfinado-Baker M, Baker EW (1982) Notes on honey bee mites of the genus Acarapis hirst (Acari: Tarsonemidae). Int J Acarol 8:211–226

    Article  Google Scholar 

  12. de Miranda JR, Cordoni G, Budge G (2010) The Acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J Invertebr Pathol 103:S30–S47

    Article  PubMed  Google Scholar 

  13. Dhaliwal HS, Srivastava S, Sharma PL (1974) Some biological observations on the mite, Acarapis woodi Rennie, infesting honeybees, Apis cerana indica F. Curr Sci 43:750–751

    Google Scholar 

  14. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97

    Article  CAS  PubMed  Google Scholar 

  16. Gisder S, Aumeier P, Genersch E (2009) Deformed wing virus: replication and viral load in mites (Varroa destructor). J Gen Virol 90:463–467

    Article  CAS  PubMed  Google Scholar 

  17. Goka K, Okabe K, Yoneda M (2006) Worldwide migration of parasitic mites as a result of bumblebee commercialization. Population Ecol 48:285–291

    Article  Google Scholar 

  18. Grabensteiner E, Ritter W, Carter MJ, Davison S, Pechhacker H, Kolodziejek J, Boecking O, Derakhshifar I, Moosbeckhofer R, Licek E, Nowotny N (2001) Sacbrood virus of the honeybee (Apis mellifera): rapid identification and phylogenetic analysis using reverse transcription–PCR. Clin Diag Lab Immunol 8:93–104

    CAS  Google Scholar 

  19. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, pp 21–132

    Chapter  Google Scholar 

  20. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  21. Kohno K, Sokabe T, Tominaga M, Kadowaki T (2010) Honey bee thermal/chemical sensor, AmHsTRPA, reveals neofunctionalization and loss of Transient Receptor Potential channel genes. J Neurosci 30:12219–12229

    Article  CAS  PubMed  Google Scholar 

  22. Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Le Gall O, Christian P, Fauquet CM, King AM, Knowles NJ, Nakashima N, Stanway G, Gorbalenya AE (2008) Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T = 3 virion architecture. Arch Virol 153:715–727

    Article  PubMed  Google Scholar 

  24. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  25. Maori E, Lavi S, Mozes-Koch R, Gantman Y, Peretz Y, Edelbaum O, Tanne E, Sela I (2007) 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 88:3428–3438

    Article  CAS  PubMed  Google Scholar 

  26. McMullan JB, Brown MJ (2009) A qualitative model of mortality in honey bee (Apis mellifera) colonies infested with tracheal mites (Acarapis woodi). Exp Appl Acarol 47:225–234

    Article  PubMed  Google Scholar 

  27. Oldroyd BP (1999) Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees. Trends Ecol Evol 14:312–315

    Article  PubMed  Google Scholar 

  28. Olson L (2006) The economics of terrestrial invasive species: a review of the literature. Agr Resource Econ Rev 35:178–194

    Google Scholar 

  29. Otterstatter MC, Thomson JD (2008) Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PLoS One 3:e2771

    Article  PubMed  PubMed Central  Google Scholar 

  30. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  PubMed  Google Scholar 

  31. Power AG, Mitchell CE (2004) Pathogen spillover in disease epidemics. Am Nat 164:S79–S89

    Article  PubMed  Google Scholar 

  32. Price MH, Proboszcz SL, Routledge RD, Gottesfeld AS, Orr C, Reynolds JD (2011) Sea louse infection of juvenile sockeye salmon in relation to marine salmon farms on Canada's west coast. PLoS One 6:e16851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ribiere M, Triboulot C, Mathieu L, Aurieres C, Faucon JP, Pepin M (2002) Molecular diagnosis of chronic bee paralysis virus infection. Apidologie 33:339–351

    Article  CAS  Google Scholar 

  34. Sammataro D, Gerson U, Needham G (2000) Parasitic mites of honey bees: life history, implications, and impact. Ann Rev Entomol 45:519–548

    Article  CAS  Google Scholar 

  35. Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, vanEngelsdorp D, Lipkin WI, Depamphilis CW, Toth AL, Cox-Foster DL (2010) RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS One 5:e14357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  37. Tapaszti Z, Forgách P, Kovágó C, Topolska G, Nowotny N, Rusvai M, Bakonyi T (2009) Genetic analysis and phylogenetic comparison of Black queen cell virus genotypes. Vet Microbiol 139:227–234

    Article  CAS  PubMed  Google Scholar 

  38. Verma LR, Rana BS, Verma S (1990) Observations on Apis cerana colonies surviving from Thai Sacbrood virus infection. Apidologie 21:169–174

    Article  Google Scholar 

Download references

Acknowledgments

TK is grateful to local beekeepers (Y. Hasada, K. Kogami, and T. Arano) and the members of Japan Beekeeping Association for collecting honey bee samples. We are greatly indebted to Yanping (Judy) Chen for valuable comments on the manuscript. This research was supported by Yamada Research Grant; The Sumitomo Foundation; Mitsui & Co., Ltd. Environment Fund, and Grant-in-Aid for Scientific Research from JSPS to TK. A part of this work was also supported by a grant from Promotion of Basic Research Activities for Innovative Biosciences (PRO-BRAIN) to MY.

Author information

Author notes

  1. Tatsuhiko Kadowaki

    Present address: Department of Biological Sciences, Xi’an Jiaotong-Liverpool University, Suzhou Industrial Park, Suzhou, 215123, Jiangsu Province, China

Authors and Affiliations

  1. Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601, Japan

    Yuriko Kojima, Taku Toki, Tomomi Morimoto & Tatsuhiko Kadowaki

  2. Honey Bee Research Group, Animal Breeding and Reproduction Research Team, National Institute of Livestock and Grassland Science, 2 Ikenodai, Tsukuba, Ibaraki, 305-0901, Japan

    Mikio Yoshiyama & Kiyoshi Kimura

Authors
  1. Yuriko Kojima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Taku Toki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tomomi Morimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mikio Yoshiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kiyoshi Kimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tatsuhiko Kadowaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tatsuhiko Kadowaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kojima, Y., Toki, T., Morimoto, T. et al. Infestation of Japanese Native Honey Bees by Tracheal Mite and Virus from Non-native European Honey Bees in Japan. Microb Ecol 62, 895–906 (2011). https://doi.org/10.1007/s00248-011-9947-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-011-9947-z

Keywords

Search

Navigation