Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-23T09:27:51.058Z Has data issue: false hasContentIssue false
  • English
  • Français

Salivary secretions from the honeybee mite, Varroa destructor: effects on insect haemocytes and preliminary biochemical characterization

Published online by Cambridge University Press:  01 February 2011

E. H. RICHARDS ,
BENJAMIN JONES  and
ALAN BOWMAN
E. H. RICHARDS*
Affiliation:
The Food and Environment Research Agency, Sand Hutton, York YO41 1LZ, UK
BENJAMIN JONES
Affiliation:
National Bee Unit, Food and Environment Research Agency, Sand Hutton, York YO41 1LZ, UK
ALAN BOWMAN
Affiliation:
School of Biological Sciences (Zoology), University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
*
*Corresponding author: The Food and Environment Research Agency, Sand Hutton, York YO41 1LZ, UK. Tel: +01904 462639. Fax: +01904 462111. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Introduction. The ectoparasitic honey bee mite Varroa destructor feeds on the haemolymph of the honey bee, Apis mellifera, through a single puncture wound that does not heal but remains open for several days. It was hypothesized that factors in the varroa saliva are responsible for this aberrant wound healing. Methods. An in vitro procedure was developed for collecting salivary gland secretions from V. destructor. Mites were incubated on balls of cotton wool soaked in a tissue culture medium (TC-100), and then induced to spit by topical application of an ethanolic pilocarpine solution. Results. Elution of secretions from balls of cotton wool, followed by electrophoretic analysis by SDS-PAGE and electroblotting indicated the presence of at least 15 distinct protein bands, with molecular weights ranging from 130 kDa to <17 kDa. Serial titration of V. destructor salivary secretions in TC-100 followed by an 18-h incubation with haemocytes from the caterpillar, Lacanobia oleracea, indicated that the secretions damage the haemocytes and suppresses their ability to extend pseudopods and form aggregates. Conclusion. We suggest that these secretions facilitate the ability of V. destructor to feed repeatedly off their bee hosts by suppressing haemocyte-mediated wound healing and plugging responses in the host.

Keywords

Varroa destructorhoney beesalivasalivary gland secretionsspithaemocytehaemocyte aggregation
Type
Research Article
Information
Parasitology , Volume 138 , Issue 5 , April 2011 , pp. 602 - 608
Copyright
© Crown Copyright. Published by Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bowman, A. S., Ball, A. and Sauer, J. R. (2008). Tick salivary glands: the physiology of tick water balance and their role in pathogen trafficking and transmission. In Ticks: Biology, Disease and Control (ed. Bowman, A. S. and Nuttall, P. A.), pp. 73–91. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Bowman, A. S. and Sauer, J. R. (2004). Tick salivary glands: function, physiology and future. Parasitology 129, S67–S81.CrossRefGoogle ScholarPubMed
Brey, P. T., Lee, W.- J., Yamakawa, M., Koizumi, Y., Perrot, S., Francois, M. and Ashida, M. (1993). Role of the integument in insect immunity: epicuticular abrasion and induction of cecropin synthesis in cuticular epithelial cells. Proceedings of the National Academy of Sciences, USA 90, 6275–6279.CrossRefGoogle ScholarPubMed
Brossard, M. and Wikel, S. K. (2004). Tick immunobiology. Parasitology 129, S161–S176.CrossRefGoogle ScholarPubMed
Campbell, E. M., Budge, G. E. and Bowman, A. S. (2010 a). Gene-knockdown in the honey bee mite Varroa destructor by a non-invasive approach: studies on a glutathione S-transferase. Parasites and Vectors 3, 73.CrossRefGoogle ScholarPubMed
Campbell, E. M., Burdin, M., Hoppler, S. and Bowman, A. S. (2010 b). Role of an aquaporin in the sheep tick Ixodes ricinus: assessment as a potential control target. International Journal for Parasitology 40, 15–23.CrossRefGoogle ScholarPubMed
Cornman, S. R., Schatz, M. C., Johnston, S. J., Chen, Y. P., Pettis, J., Hunt, G., Bourgeois, L., Elsik, C., Anderson, D., Grozinger, C. M. and Evans, J. D. (2010). Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera. BMC Genomics 11, 602.CrossRefGoogle Scholar
De D'Aubeterre, J. P., Myrold, D. D., Royce, L. A. and Rossignol, P. A. (1999). A scientific note of an application of isotope ratio mass spectrometry to feeding by the mite, Varroa jacobsoni Oudemans, on the honeybee, Apis mellifera L. Apidologie 30, 351–352.Google Scholar
de Miranda, J. R. and Genersch, E. (2010). Deformed wing virus. Journal of Invertebrate Pathology 103, S48–S61.CrossRefGoogle ScholarPubMed
Dushay, M. S. (2009). Insect hemolymph clotting. Cell. Mol. Life Sci. 66, 2643–2650.Google ScholarPubMed
Garedew, A., Schmolz, E. and Lamprecht, I. (2004). The energy and nutritional demand of the parasitic life of the mite Varroa destructor. Apidologie 35, 419–430.CrossRefGoogle Scholar
Gillespie, J. P., Kanost, M. R. and Trenczek, T. (1997). Biological mediators of insect immunity. Annual Review of Entomology 42, 611–643.CrossRefGoogle ScholarPubMed
Gregory, P. G., Evans, J. D., Rinderer, T. and De Guzman, L. (2005). Conditional immune-gene suppression of honeybees parasitized by Varroa mites. Journal of Insect Science 5, 1–5.CrossRefGoogle ScholarPubMed
Herrmann, M., Kanbar, G. and Engels, W. (2005). Survival of honey bee (Apis mellifera) pupae after trypan blue staining of wounds caused by Varroa destructor mites or artificial perforation. Apidologie 36, 107–111.CrossRefGoogle Scholar
Jones, L. D., Davies, C. R., Steele, G. M. and Nuttall, P. A. (1987). A novel mode of arbovirus transmission involving a nonviremic host. Science 237, 775–777.CrossRefGoogle ScholarPubMed
Kanbar, G. and Engels, W. (2003). Ultrastructure and bacterial infection of wounds in honey bee (Apis mellifera) pupae punctured by Varroa mites. Parasitology Research 90, 349–354.CrossRefGoogle ScholarPubMed
Kanbar, G. and Engels, W. (2005). Communal use of integumental wounds in honey bee (Apis mellifera) pupae multiply infested by the ectoparasitic mite Varroa destructor. Genetics and Molecular Research 4, 465–472.Google ScholarPubMed
Klein, A., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C. and Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society of London, B 274, 303–313.Google ScholarPubMed
Labuda, M., Jones, L. D., Williams, T. and Nuttall, P. A. (1993). Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts. Medical and Veterinary Entomology 7, 193–196.CrossRefGoogle ScholarPubMed
Martin, S. J. (2004). Acaricide (pyrethroid) resistance in Varroa destructor. Bee World 85, 67–69.CrossRefGoogle Scholar
Nuttall, P. A. and Labuda, M. (2004). Tick-host interactions: saliva-activated transmission. Parasitology 129, S177–S189.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. C. (1995). Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infectious Agents and Disease 4, 143–152.Google ScholarPubMed
Ribeiro, J. M. C. and Francischetti, I. M. B. (2003). Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annual Review of Entomology 48, 73–88.CrossRefGoogle ScholarPubMed
Richards, E. H. and Dani, M. P. (2008). Biochemical isolation of an insect haemocyte anti-aggregation protein from the venom of the endoparasitic wasp, Pimpla hypochondriaca, and identification of its gene. Journal of Insect Physiology 54, 1041–1049.CrossRefGoogle ScholarPubMed
Richards, E. H. and Edwards, J. P. (2001). Proteins synthesized and secreted by larvae of the ectoparasitic wasp, Eulophus pennicornis. Archives of Insect Biochemistry and Physiology 46, 140–151.CrossRefGoogle ScholarPubMed
Richards, E. H. and Edwards, J. P. (2002). Larvae of the ectoparasitic wasp, Eulophus pennicornis, release factors which adversely affect haemocytes of their host, Lacanobia oleracea. Journal of Insect Physiology 48, 845–855.CrossRefGoogle ScholarPubMed
Rosenkranz, P., Aumeier, P. and Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology 103, S96–S119.CrossRefGoogle ScholarPubMed
Shen, M., Cui, L., Ostiguy, N. and Cox-Foster, D. (2005 a). Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. Journal of General Virology 86, 2281–2289.CrossRefGoogle ScholarPubMed
Shen, M., Yang, X., Cox-Foster, D. and Cui, L. (2005 b). The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology 342, 141–149.CrossRefGoogle Scholar
Tewarson, N. C., Singh, A. and Engels, W. (1992). Reproduction of Varroa jacobsoni in colonies of Apis cerana indica under natural and experimental conditions. Apidologie 23, 161–171.CrossRefGoogle Scholar
Titus, R. G., Bishop, J. V. and Mejia, J. S. (2006). The immunomodulatory factors of arthropod saliva and the potential for these factors to serve as vaccine targets to prevent pathogen transmission. Parasite Immunology 28, 131–141.CrossRefGoogle ScholarPubMed
Theopold, U., Li, D., Fabbri, M., Scherfer, C. and Schmidt, O. (2002). The coagulation of insect hemolymph. Cell and Molecular Life Sciences 59, 363–372.CrossRefGoogle ScholarPubMed
Valenzuela, J. G. (2004). Exploring tick saliva: from biochemistry to ‘sialomes’ and functional genomics. Parasitology 129, S83–S94.CrossRefGoogle ScholarPubMed
Yang, X. and Cox-Foster, D. L. (2005). Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proceedings of the National Academy of Sciences, USA 102, 7470–7475.CrossRefGoogle ScholarPubMed