DOI QR코드

DOI QR Code

Controlling Sacbrood Virus Disease in Apis cerana Colonies with Biological Methods in Korea

  • Vung, Nguyen Ngoc (Department of Agricultural Biology, National Institute of Agricultural Sciences, RDA) ;
  • Kim, Iksoo (College of Agriculture & Life Sciences, Chonnam National University) ;
  • Lee, Man Young (Department of Agricultural Biology, National Institute of Agricultural Sciences, RDA) ;
  • Kim, Hye Kyung (Department of Industrial Entomology, Korea National College of Agriculture and Fisheries) ;
  • Kim, Dong Won (Department of Agricultural Biology, National Institute of Agricultural Sciences, RDA) ;
  • Choi, Yong Soo (Department of Agricultural Biology, National Institute of Agricultural Sciences, RDA)
  • Received : 2018.11.04
  • Accepted : 2018.11.27
  • Published : 2018.11.30

Abstract

As Sacbrood virus (SBV), a causative agent of larval death and colony collapse in Apis cerana honey bee, is prevalent and poses one of the most significant threats to the Korean apiculture, development of methods to counter this viral disease is urgently needed. In this study we tested some SBV controlling methods, such as requeen, shook swam, adding Apis mellifera and spraying yogurt to SBV inoculated colony. Colony size measured by number of sealed brood and adult were evaluated every 15 days until two months while instances of recurrence were recorded up to five months after applying treatment methods. We also test the effects of yogurt on healthy and SBV-infected larvae at both in vitro reared larvae and colony level. Our result showed that all SBV controlling methods had similar success rates with respect to elimination of SBV clinical symptom up to 30 days post treatment. Mix-species and spraying yogurt method had similar pattern of sealed brood and adult number and higher than that of other SBV controlling methods up to 45 days post treatment. These two groups also showed the lower percentage of SBV recurrence (50% and 66.7%) at 120 days post treatment than other group that mostly colony had clinical symptom. Result on in vitro reared larvae challenged with yogurt showed that yogurt have neither harmless on healthy larvae nor remedial effect on SBV infected larvae. However, at colony level, colony in group received yogurt treatment removed significantly more SBV-infected larvae, SBV-killed larvae, and even healthy larvae in comparison to the control, suggested that yogurt could trigger the hygienic behavior of nurse bee. Our results recommended that it is practical in beekeeping by adding A. mellifera and spraying yogurt to control SBV in A. cerana colony.

Keywords

Acknowledgement

Supported by : National Institute of Agricultural Sciences

References

  1. Ahn, A. J., K. S. Ahn, G. H. Suh, J. H. Noh, Y. H. Kim, et al. 2015. Efficacy of silver ions against Sacbrood virus infection in the Eastern honey bee Apis cerana. J. Vet. Sci. 16: 289-295. https://doi.org/10.4142/jvs.2015.16.3.289
  2. Ai, H., X. Yan and R. Han. 2012. Occurrence and prevalence of seven bee viruses in Apis mellifera and Apis cerana apiaries in China. J. Invertebr. Pathol. 109: 160-164. https://doi.org/10.1016/j.jip.2011.10.006
  3. Anderson, D. L.1995. Viruses of Apis cerana and Apis mellifera, The Asiatic hive bee: Apiculture, biology, and role in sustainable development in tropical and subtropical Asia, Enviroquest Ltd., Cambridge, Ontario, Canada, pp. 160-171.
  4. Anderson, D. L. and H. Giacon. 1992. Reduced pollen collection by honey bee (Hymenoptera: Apidae) colonies infected with Nosema apis and sacbrood virus. J. Econ. Entomol. 85: 47-51. https://doi.org/10.1093/jee/85.1.47
  5. Arathi, H. and M. Spivak. 2001. Influence of colony genotypic composition on the performance of hygienic behaviour in the honeybee, Apis mellifera L. Animal Behaviour 62: 57-66. https://doi.org/10.1006/anbe.2000.1731
  6. Arathi, H. S., I. Burns and M. Spivak. 2000. Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioural repertoire of hygienic bees. Ethol 106: 365-379. https://doi.org/10.1046/j.1439-0310.2000.00556.x
  7. Aruna, R., M. R. Srinivasan and R. Selvarajan. 2017. Efficacy of plant products on sacbrood virus attacking Apis cerana indica Fabricius. J. Entomol. Zool. Stud.
  8. Bailey, L. and E. F. W. Fernando. 1972. Effects of sacbrood virus on adult honeybees. Ann. Appl. Biol. 72: 27-35. https://doi.org/10.1111/j.1744-7348.1972.tb01268.x
  9. Bailey, L., A. J. Gibbs and R. D. Woods. 1964. Sacbrood virus of the larval honey bee (Apis mellifera Linnaeus). Virol 23: 425-429. https://doi.org/10.1016/0042-6822(64)90266-1
  10. Baker, A. C. and D. C. Schroeder. 2008. The use of RNAdependent RNA polymerase for the taxonomic assignment of Picorna-like viruses (order Picornavirales) infecting Apis mellifera L. populations. Virol. J. 5: 10. https://doi.org/10.1186/1743-422X-5-10
  11. Beshers, S. N. and J. H. Fewell. 2001. Models of division of labor in social insects. Ann Rev Entom 46: 413-440. https://doi.org/10.1146/annurev.ento.46.1.413
  12. Chen, Y., Y. Zhao, J. Hammond, H. T. Hsu, J. Evans, et al. 2004. Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J. Invertebr. Pathol. 87: 84-93. https://doi.org/10.1016/j.jip.2004.07.005
  13. Choe, S. E., T. T. D. Nguyen, B. H. Hyun, J. H. Noh, H. S. Lee, et al. 2012. Genetic and phylogenetic analysis of South Korean sacbrood virus isolates from infected honey bees (Apis cerana). Veterinary microbiology 157: 32-40. https://doi.org/10.1016/j.vetmic.2011.12.007
  14. Choi, Y. S., M. Y. Lee, I. P. Hong, N. S. Kim, H. K. Kim, et al. 2010. Occurrence of sacbrood virus in Korean apiaries from Apis cerana (Hymenoptera: Apidae). Korean J. Apiculture 25: 187-191.
  15. Crailsheim, K., R. Brodschneider, P. Aupinel, D. Behrens, E. Genersch, et al. 2013. Standard methods for artificial rearing of Apis mellifera larvae. J. Apic. Res. 52: 1-16.
  16. Cremer, S., C. D. Pull and M. A. Furst. 2018. Social immunity: Emergence and evolution of colony-level disease protection. Annu. Rev. Entomol. 63: 105-123. https://doi.org/10.1146/annurev-ento-020117-043110
  17. Cremer, S. and M. Sixt. 2009. Analogies in the evolution of individual and social immunity. Philos. Trans. R. Soc. London. B: Biol. Sci. 364: 129-142. https://doi.org/10.1098/rstb.2008.0166
  18. Crowley, S., J. Mahony and D. van Sinderen. 2013. Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci Technol 33: 93-109.
  19. Desai, S. D. and R. W. Currie. 2016. Effects of wintering environment and parasite-pathogen interactions on honey bee colony loss in North Temperate regions. PloS one 11: e0159615. https://doi.org/10.1371/journal.pone.0159615
  20. Dicks, L. and M. Botes. 2009. Probiotic lactic acid bacteria in the gastro-intestinal tract: health benefits, safety and mode of action. Benef Microbes 1: 11-29.
  21. Evans, J. D., K. Aronstein, Y. P. Chen, C. Hetru, J. L. Imler, et al. 2006. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15: 645-656. https://doi.org/10.1111/j.1365-2583.2006.00682.x
  22. Forsgren, E., T. C. Olofsson, A. Vaasquez and I. Fries. 2010. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41: 99-108. https://doi.org/10.1051/apido/2009065
  23. Gong, H.-R., X.-X. Chen, Y. P. Chen, F.-L. Hu, J.-L. Zhang, et al. 2016. Evidence of Apis cerana Sacbrood virus infection in Apis mellifera. Appl. Environ. Microbiol. 82: 2256-2262. https://doi.org/10.1128/AEM.03292-15
  24. Gramacho, K. P. and M. Spivak. 2003. Differences in olfactory sensitivity and behavioral responses among honey bees bred for hygienic behavior. Behav. Ecol. Sociobiol. 54: 472-479. https://doi.org/10.1007/s00265-003-0643-y
  25. Guler, A. 2008. The effects of the shook swarm technique on honey bee (Apis mellifera L.) colony productivity and honey quality. J. Apic. Res. 47: 27-34. https://doi.org/10.1080/00218839.2008.11101420
  26. Hansen, H. and C. J. Brodsgaard. 2003. Control of American foulbrood by the shaking method. Apiacta 38: 140-145.
  27. Jung, C. and S. K. Cho. 2015. Relationship between honeybee population and honey production in Korea. Korean J. Apiculture 30: 7-12. https://doi.org/10.17519/apiculture.2015.04.30.1.7
  28. Killer, J., S. Dubna, I. Sedlacek and P. Svec. 2014. Lactobacillus apis sp. nov., from the stomach of honeybees (Apis mellifera), having an in vitro inhibitory effect on the causative agents of American and European foulbrood. Int. J. Syst. Evol. Microbiol. 64: 152-157. https://doi.org/10.1099/ijs.0.053033-0
  29. Klein, A.-M., B. E. Vaissiere, J. H. Cane, I. Steffan-Dewenter, S. A. Cunningham, et al. 2007. Importance of pollinators in changing landscapes for world crops. Proceeding of the Royal Society of London B: Biological Sciences 274: 303-313. https://doi.org/10.1098/rspb.2006.3721
  30. Leclercq, G., B. Pannebakker, N. Gengler, B. K. Nguyen and F. Francis. 2017. Drawbacks and benefits of hygienic behavior in honey bees (Apis mellifera L.): a review. J. Apic. Res. 56: 366-375. https://doi.org/10.1080/00218839.2017.1327938
  31. Machado, T. A. D. G., M. E. G. de Oliveira, M. I. F. Campos, P. O. A. de Assis, E. L. de Souza, et al. 2017. Impact of honey on quality characteristics of goat yogurt containing probiotic Lactobacillus acidophilus. LWT-Food Science and Technology 80: 221-229. https://doi.org/10.1016/j.lwt.2017.02.013
  32. Mondet, F., S. H. Kim, J. R. De Miranda, D. Beslay, Y. Le Conte, et al. 2016. Specific cues associated with honey bee social defence against Varroa destructor infested brood. Sci Rep 6: 25444. https://doi.org/10.1038/srep25444
  33. Nazzi, F., S. P. Brown, D. Annoscia, F. Del Piccolo, G. Di Prisco, et al. 2012. Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 8: e1002735. https://doi.org/10.1371/journal.ppat.1002735
  34. Oldroyd, B. P. and S. Wongsiri. 2006. Asian honey bees: biology, conservation, and human interactions. Harvard University Press.
  35. Oxley, P. R., M. Spivak and B. P. Oldroyd. 2010. Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol. Ecol. 19: 1452-1461. https://doi.org/10.1111/j.1365-294X.2010.04569.x
  36. Palacio, M. A., E. Rodriguez, L. Goncalves, E. Bedascarrasbure and M. Spivak. 2010. Hygienic behaviors of honey bees in response to brood experimentally pin-killed or infected with Ascosphaera apis. Apidologie 41: 602-612. https://doi.org/10.1051/apido/2010022
  37. Peng, Y.-S., Y. Fang, S. Xu and L. Ge. 1987. The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite, Varroa jacobsoni Oudemans. J. Invertebr. Pathol. 49: 54-60. https://doi.org/10.1016/0022-2011(87)90125-X
  38. Pratt, S. C. 2004. Collective control of the timing and type of comb construction by honey bees (Apis mellifera). Apidologie 35: 193-205. https://doi.org/10.1051/apido:2004005
  39. Rashid, M. and M. Sultana. 2016. Role of probiotics in human and animal health review. J. Prob. Health 4: 2-4.
  40. Rothenbuhler, W. C. 1964. Behavior genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood. Am. Zool. 4: 111-123. https://doi.org/10.1093/icb/4.2.111
  41. Spivak, M. and M. Gilliam. 1993. Facultative expression of hygienic behaviour of honey bees in relation to disease resistance. J. Apic. Res. 32: 147-157. https://doi.org/10.1080/00218839.1993.11101300
  42. Spivak, M. and M. Gilliam. 1998. Hygienic behaviour of honey bees and its application for control of brood diseases and Varroa: Part II. Studies on hygienic behaviour since the Rothenbuhlerera. Bee world 79: 169-186. https://doi.org/10.1080/0005772X.1998.11099408
  43. Spivak, M. and G. S. Reuter. 2001. Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie 32: 555-565. https://doi.org/10.1051/apido:2001103
  44. Sun, L., M. Li, D. Fei, J. Wang, L. Li, et al. 2018. Preparation and application of egg yolk antibodies against Chinese sacbrood virus infection. Frontiers in microbiology 9: 1814. https://doi.org/10.3389/fmicb.2018.01814
  45. Swanson, J. A., B. Torto, S. A. Kells, K. A. Mesce, J. H. Tumlinson, et al. 2009. Odorants that induce hygienic behavior in honeybees: identification of volatile compounds in chalkbrood-infected honeybee larvae. J. Chem. Ecol. 35: 1108-1116. https://doi.org/10.1007/s10886-009-9683-8
  46. Tentcheva, D., L. Gauthier, N. Zappulla, B. Dainat, F. Cousserans, et al. 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. https://doi.org/10.1128/AEM.70.12.7185-7191.2004
  47. Theisen-Jones, H. and K. Bienefeld. 2016. The Asian honey bee (Apis cerana) is significantly in decline. Bee World 93: 90-97. https://doi.org/10.1080/0005772X.2017.1284973
  48. Thompson, H. M., R. J. Waite, S. Wilkins, M. A. Brown, T. Bigwood, et al. 2006. Effects of shook swarm and supplementary feeding on oxytetracycline levels in honey extracted from treated colonies. Apidologie 37: 51-57. https://doi.org/10.1051/apido:2005058
  49. Toan, T. V., M. L. Lee, H. S. Sim, H. K. Kim, G. H. Byuon, et al. 2014. Biological mitigation of Sacbrood disease on Apis cerana colonies. Korean J. Apiculture 29: 181-186.
  50. Toan, T. V., M. L. Lee, H. S. Sim, H. K. Kim, G. H. Byuon, et al. 2014. Initial results of rearing honey bee Apis cerana in vitro. Korean J. Apiculture 29: 193-197.
  51. Vasquez, A., E. Forsgren, I. Fries, R. J. Paxton, E. Flaberg, et al. 2012. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PloS one 7: e33188. https://doi.org/10.1371/journal.pone.0033188
  52. Vasquez, A. and T. C. Olofsson. 2009. The lactic acid bacteria involved in the production of bee pollen and bee bread. J. Apic. Res. 48: 189-195. https://doi.org/10.3896/IBRA.1.48.3.07
  53. Verma, S. and P. K. Attri. 2008. Indigenous beekeeping for sustainable development in Himachal Himalaya. Indian Journal of Traditional Knowledge 7: 221-225.
  54. Wagoner, K. M., M. Spivak and O. Rueppell. 2018. Brood affects hygienic behavior in the honey bee (Hymenoptera: Apidae). J Econ Ento.
  55. Waite, R. J., M. A. Brown, H. M. Thompson and M. H. Bew. 2003. Controlling European foulbrood with the shook swarm method and oxytetracycline in the UK. Apidologie 34: 569-575. https://doi.org/10.1051/apido:2003052
  56. Webster, T. C., Y. S. Peng and S. S. Duffey. 1987. Conservation of nutrients in larval tissue by cannibalizing honey bees. Physiol. Entomol. 12: 225-231. https://doi.org/10.1111/j.1365-3032.1987.tb00745.x
  57. Wu, M., Y. Sugimura, N. Takaya, D. Takamatsu, M. Kobayashi, et al. 2013. Characterization of bifidobacteria in the digestive tract of the Japanese honeybee, Apis cerana japonica. J. Invertebr. Pathol. 112: 88-93. https://doi.org/10.1016/j.jip.2012.09.005
  58. Xu, P., M. Shi and X. X. Chen. 2009. Antimicrobial peptide evolution in the Asiatic honey bee Apis cerana. PLoS one 4: e4239. https://doi.org/10.1371/journal.pone.0004239
  59. Yang, M.-X., K. Tan, S. E. Radloff, C. W. Pirk and H. R. Hepburn. 2010. Hetero-specific queen retinue behavior of worker bees in mixed-species colonies of Apis cerana and Apis mellifera. Apidologie 41: 54-61. https://doi.org/10.1051/apido/2009047

Cited by

  1. Genetic and phylogenetic analysis of the honey bee sacbrood virus from jiangxi isolates vol.25, pp.1, 2018, https://doi.org/10.1016/j.aspen.2021.101847