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Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge

Published online by Cambridge University Press:  02 November 2006

X. YANG  and
D. COX-FOSTER
X. YANG
Affiliation:
501 ASI Building, Department of Entomology, Pennsylvania State University, University Park, PA 16802, USA
D. COX-FOSTER
Affiliation:
501 ASI Building, Department of Entomology, Pennsylvania State University, University Park, PA 16802, USA
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Abstract

Varroa mites (Varroa destructor) are serious ectoparasites of honey bees (Apis mellifera). This research addresses the impact of varroa mites on survivorship, viral incidence, and physiological traits of newly-emerged worker bees. RT-PCR confirmed our previous finding that varroa parasitization was linked to high levels of deformed wing virus (DWV). In non-treatment bees, varroa parasitization combined with increased viral levels altered survivorship curves from long-survival to shorter-survival types. After challenge with live Escherichia coli, the survivorship of mite-parasitized bees was significantly lower than mite-free bees. Deformed-wing, mite-parasitized bees died on average within 1 day, even without E. coli challenge. This was correlated with the absence of an important enzyme activity in insect immunity, phenol oxidase, lacking even in those bees challenged with immuno-elicitors. The lack of inducible phenol oxidase activity indicated that the bee immune system is not fully competent upon adult emergence. Varroa parasitism also significantly reduced body weight of the parasitized bees, but body weight was not significantly correlated with the survivorship of mite-parasitized bees. Our research indicates that the combination of mite parasitization, the interaction of DWV and microbes, and a developmental immune incompetency attribute to decreased worker survivorship and have a negative impact on colony fitness.

Keywords

Apis melliferaVarroa destructorsurvivorshipdeformed wing virusphenol oxidaseimmunity
Type
Research Article
Information
Parasitology , Volume 134 , Issue 3 , March 2007 , pp. 405 - 412
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Allen, M. F., Ball, R. F., White, R. F. and Antoniw, J. F. ( 1986). The detection of acute paralysis virus in Varroa jacobsoni by the use of a simple indirect ELISA. Journal of Apicultural Research 15, 100–105.CrossRefGoogle Scholar
Anderson, D. L. and Gibbs, A. J. ( 1988). Inapparent virus infections and their interaction in pupae of honey bee (Apis mellifera Linnaeus) in Australia. Journal of General Virology 69, 1617–1625.CrossRefGoogle Scholar
Ashida, M. and Yamazaki, H. I. ( 1990). Biochemistry of the phenoloxidase system in insect: with special reference to its activation. In Molting and Metamorphosis ( ed. Ohnishi, E. and Ishizaki, H.), pp. 239–265. Japanese Science Society Press, Tokyo.
Bailey, L. and Ball, B. V. ( 1991). Honey Bee Pathology, 2nd Edn. Academic Press, San Diego.
Ball, B. V. and Allen, M. F. ( 1988). The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni. Annals of Applied Biology 113, 237–244.CrossRefGoogle Scholar
Bowen-Walker, P. L., Martin, S. J. and Gunn, A. ( 1999). The transmission of deformed-wing virus between honey bees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. Journal of Invertebrate Pathology 73, 101–106.Google Scholar
Camazine, S. and Liu, T. P. ( 1997). Virus-like particles associated with the mite, Varroa jacobsoni. Journal of Invertebrate Pathology 71, 177–178.Google Scholar
Cox-Foster, D. L. and Stehr, J. E. ( 1994). Induction and localization of FAD-glucose dehydrogenase (GLD) during encapsulation of abiotic implants in Manduca sexta larvae. Journal of Insect Physiology 40, 235–249.CrossRefGoogle Scholar
De Jong, D., Morse, R. A. and Eickwort, G. C. ( 1982). Mite pests of honey bees. Annual Review of Entomology 27, 229–252.CrossRefGoogle Scholar
Finley, J., Camazine, S. and Frazier, M. ( 1996). The epidemic of honey bee colony losses during the 1995–1996 season. Apicultural Research 136, 805–808.Google Scholar
Free, J. B. ( 1957). The transmission of food between worker honeybees. British Journal of Animal Behaviour 5, 41–47.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 Scholar
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 Scholar
Kovac, H. and Crailsheim, K. ( 1988). Lifespan of Apis mellifera Carnica Polle. Infested by Varroa jacobsoni Oud. in relation to season and extent of infestation. Journal of Apicultural Research 27, 230–238.Google Scholar
Mikawa, F. ( 1986). A study on the extermination of Varroa jacobsoni. Proceedings of the XXXth International Congress of Apiculture (1986) pp. 178–179.
Mobus, B. and de Bruyn, C. ( 1993). The New Varroa Handbook. Arc and Throstle Press, Todmorden.
Moret, Y. and Schmid-Hempel, P. ( 2001). Immune defence in bumble-bee offspring. Nature, London 414, 506.CrossRefGoogle Scholar
Morse, R. A. and Calderone, N. W. ( 2000). The value of honey bee as pollinators of U.S. crops in 2000. Bee Culture 128, 1–15.Google Scholar
Morse, R. A. and Flottum, K. ( 1997). Honey Bee Pests, Predators, and Diseases, 3rd Edn. A. I. Root Co. Medina, Ohio.
Ohashi, K., Natori, S. and Kubo, T. ( 1999). Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of the worker honeybee (Apis mellifera L.). European Journal of Biochemistry 265, 127–133.CrossRefGoogle Scholar
Ratcliffe, N. A., Leonard, C. and Rowley, A. F. ( 1984). Prophenol oxidase activation: nonself recognition and cell cooperation in insect immunity. Science 226, 557–559.CrossRefGoogle Scholar
Sammataro, D., Gerson, U. and Needham, G. R. ( 2000). Parasitic mites of honey bee: life history, implications and impact. Annual Review of Entomology 45, 517–546.Google Scholar
Sano, O., Kunikata, T., Kohno, K., Iwaki, K., Ikeda, M. and Kurimoto, M. ( 2004). Characterization of royal jelly proteins in both Africanized and European honeybees (Apis mellifera) by two-dimensional gel electrophoresis. Journal of Agricultural Food Chemistry 52, 15–20.CrossRefGoogle Scholar
Santos, K. S., dos Santos, L. D., Mendes, M. A., de Souza, B. M., Malaspina, O. and Palma, M. S. ( 2005). Profiling the proteome complement of the secretion from hypopharyngeal gland of Africanized nurse-honeybees (Apis mellifera L.). Insect Biochemistry and Molecular Biology 35, 85–91.CrossRefGoogle Scholar
Schowalter, T. D. ( 2000). Insect Ecology. Academic Press, London.
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.Google Scholar
Shen, M., Yang, X., Cox-Foster, D. L. 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.Google Scholar
Shimanuki, H., Calderone, N. W. and Knox, D. A. ( 1994). Parasitic mite syndrome – the symptoms. American Bee Journal 134, 827–828.Google Scholar
Tong, Y., Jiang, H. and Kanost, M. R. ( 2005). Identification of plasma proteases inhibited by Manduca sexta serpin-4 andserpin-5 and their association with components of the prophenol oxidase activation pathway. Journal of Biological Chemistry 280, 14932–14942.CrossRefGoogle Scholar
Vincent, R. and Nadeau, D. ( 1983). A micromethod for the quantitation of cellular proteins in percoll with the coomassie blue dye-binding assay. Analytical Biochemistry 135, 355–362.CrossRefGoogle Scholar
Winston, M. L. ( 1987). The Biology of the Honey Bee. Harvard University Press, Cambridge, Massachusetts.
Yang, X. ( 2004). Effects of varroa mites on the immune system and pathology of honey bees. Ph.D. thesis. The Pennsylvania State University, University Park, Pennsylvania, USA.
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 National Academy of Sciences, USA 102, 7470–7475.CrossRefGoogle Scholar
Yue, C. and Genersch, E. ( 2005). RT-PCR analysis of deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). Journal of General Virology 86, 3419–3424.CrossRefGoogle Scholar