Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-25T02:50:34.487Z Has data issue: false hasContentIssue false

Supplementing with vitamin C the diet of honeybees (Apis mellifera carnica) parasitized with Varroa destructor: effects on antioxidative status

Published online by Cambridge University Press:  28 January 2014

MAREK FARJAN
Affiliation:
Biochemistry Department, Faculty of Biology and Biotechnology, University of Warmia and Mazury, Oczapowskiego 1A Str., 10-719 Olsztyn, Poland
ELŻBIETA ŁOPIEŃSKA-BIERNAT
Affiliation:
Biochemistry Department, Faculty of Biology and Biotechnology, University of Warmia and Mazury, Oczapowskiego 1A Str., 10-719 Olsztyn, Poland
ZBIGNIEW LIPIŃSKI
Affiliation:
Institute of Animal Reproduction and Food Research of Polish Academy of Sciences, Bydgoska Str. 1/8, 10-243 Olsztyn, Poland
MAŁGORZATA DMITRYJUK
Affiliation:
Biochemistry Department, Faculty of Biology and Biotechnology, University of Warmia and Mazury, Oczapowskiego 1A Str., 10-719 Olsztyn, Poland
KRYSTYNA ŻÓŁTOWSKA*
Affiliation:
Biochemistry Department, Faculty of Biology and Biotechnology, University of Warmia and Mazury, Oczapowskiego 1A Str., 10-719 Olsztyn, Poland
*
* Corresponding author. Biochemistry Department, Faculty of Biology and Biotechnology, University of Warmia and Mazury, Oczapowskiego 1A Str., 10-719 Olsztyn, Poland. E-mail: [email protected]

Summary

We studied a total of eight developmental stages of capped brood and newly emerged workers of Apis mellifera carnica colonies naturally parasitized with Varroa destructor. During winter and early spring four colonies were fed syrup containing 1·8 mg vitamin C kg−1 (ascorbic acid group; group AA) while four colonies were fed syrup without the vitamin C (control group C). Selected elements of the antioxidative system were analysed including total antioxidant status (TAS), glutathione content and antioxidative enzyme activities (superoxide dismutase, catalase, peroxidase and glutathione S-transferase). Body weight, protein content and indices of infestation were also determined. The prevalence (8·11%) and intensity (1·15 parasite per bee) of the infestation were lower in group AA compared with group C (11·3% and 1·21, respectively). Changes in the indicators of antioxidative stress were evidence for the strengthening of the antioxidative system in the brood by administration of vitamin C. In freshly emerged worker bees of group AA, despite the infestation, protein content, TAS, and the activity of all antioxidative enzymes had significantly higher values in relation to group C.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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

Aebi, H. E. (1983). Catalase. In Methods of Enzymatic Analysis, Vol. 3 (ed. Bergmeyer, H. V.), pp. 277282. Verlag Chemie, Weinheim, Germany.Google Scholar
Berger, M. M. (2005). Can oxidative damage be treated nutritionally? Clinical Nutrition 24, 172183. doi: 10.1016/j.clnu.2004.10.003.CrossRefGoogle ScholarPubMed
Bowen-Walker, P. L. and Gunn, A. (2001). The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels. Entomologia Experimentalis et Applicata 101, 207217. doi: 10.1046/j.1570-7458.2001.00905.x.Google Scholar
Bradford, M. M. (1976). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Analytical Biochemistry 72, 248254. doi: 10.1016/0003-2697(76)90527-3.Google Scholar
Chance, B. and Maehly, A. C. (1955). Assay of catalases and peroxidases. In Methods in Enzymology, Vol. 2 (ed. Colowick, S. P. and Kaplan, N.), pp. 764775. Academic Press, New York, NY, USA.Google Scholar
Clarkson, P. M. and Thompson, H. S. (2000). Antioxidants: what role do they play in physical activity and health? American Journal of Clinical Nutrition 72 (Suppl.), 637S646S.Google Scholar
Claudianos, C., Ranson, H., Johanson, R. M., Biswas, S., Schuler, M. A., Barenbaum, M. R., Feyereisen, R. and Oakeshott, J. G. (2006). A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Molecular Biology 15, 615636. doi: 10.1111/j.1365-2583.2006.00672.x.Google Scholar
Corona, M. and Robinson, G. E. (2006). Genes of the antioxidant system of honey bee: annotation and phylogeny. Insect Molecular Biology 15, 687701. doi: 10.1111/j.1365-2583.2006.00695.x.Google Scholar
Duay, P. D., De Jong, D. and Engels, W. (2003). Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites. Apidologie 34, 6165. doi: 10.1051/apido:2002052.Google Scholar
Ebert, T. A., Kevan, P. G., Bishop, B. L., Kevan, S. D. and Downer, R. A. (2007). Oral toxicity of essential oils and organic acids fed to honey bees (Apis mellifera). Journal of Apicultural Research 46, 220224. doi: 10.3896/IBRA.1.46.4.02.CrossRefGoogle Scholar
Ellman, G. L. (1959). Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 82, 7077. doi: 10.1016/0003-9861(59)90090-6.Google Scholar
Farjan, M., Dmitryjuk, M., Lipiński, Z., Łopieńska-Biernat, E. and Żółtowska, K. (2012). The supplementation with vitamin C honeybee diet: I. The effect on antioxidative system of Apis mellifera carnica brood. Journal of Apicultural Research 51, 263270. doi: 10.3896/IBRA.1.51.3.07.Google Scholar
Francis, R. M., Nielsen, S. L. and Kryger, P. (2013). Varroa–virus interaction in collapsing honey bee colonies. PLoS ONE 8, e57540. doi: 10.1371/journal.pone.0057540.Google Scholar
Ghezzi, P. (2011). Role of glutathione in immunity and inflammation in the lung. International Journal of General Medicine 4, 105113. doi: 10.2147/IJGM.S15618.Google Scholar
Gliński, Z. and Jarosz, J. (1988). Varroa jacobsoni invasion and the level of cell-free immunity in upright larvae of the worker honey bee, Apis mellifera . Folia Veterinaria 32, 3950.Google Scholar
Gliński, Z. and Jarosz, J. (1992). Varroa jacobsoni as a carrier of bacterial infections to a recipient bee host. Apidologie 23, 2531. doi: 10.1051/apido:19920103.Google Scholar
Hadaś, E. and Stankiewicz, M. (1998). Superoxide dismutase and total antioxidant status of larvae and adults of Trichostrongylus colubriformis, Haemonchus contortus and Ostertagia circumcinta . Parasitological Research 84, 646650.Google Scholar
Halliwell, B. (2011). Free radicals and antioxidants – Quo vadis? Trends in Pharmacological Sciences 32, 125130. Doi: 10.1016/j.tips.2010.12.002.Google Scholar
Harz, M., Müller, F. and Rademacher, E. (2010). Organic acids: acute toxicity on Apis mellifera and recovery in the haemolymph. Journal of Apicultural Research 49, 9596. doi: 10.3896/IBRA.1.49.1.14.Google Scholar
Jay, C. S. (1962). Colour changes in honeybee pupae. Bee World 43, 119122.Google Scholar
Jay, C. S. (1963). The development of honeybees in their cells. Journal of Apicultural Research 2, 117134.CrossRefGoogle Scholar
Karazafiris, E., Tananaki, Ch., Menkissoglu-Spiroudi, U. and Hrasyvoulou, A. (2008). Residue distribution of the acaricide coumaphos in honey following application of a new slow-release formulation. Pest Management Science 64, 165171. doi: 10.1002/ps.1493.Google Scholar
Kostaropoulos, I., Mantzari, A. E. and Papadopoulos, A. I. (1996). Alterations of some glutathione S-transferase characteristics during the development of Tenebrio molitor (Insecta: Coleoptera). Insect Biochemistry and Molecular Biology 26, 963969. doi: 10.1016/S0965-1748(96)00063-X.Google Scholar
Lipiński, Z. and Szubstarski, J. (2007). Resistance of Varroa destructor to most commonly used synthetic acaricides. Polish Journal of Veterinary Society 10, 289294.Google ScholarPubMed
Lipiński, Z. and Żółtowska, K. (2005). Preliminary evidence associating oxidative stress in honey bee drone brood with Varroa destructor . Journal of Apicultural Research 44, 126128. doi: 10.3896/IBRA.1.44.3.08.Google Scholar
Maggi, M. D., Ruffinengo, S. R., Mendoza, Y., Ojeda, P., Ramallo, G., Floris, I. and Eguaras, M. J. (2011). Susceptibility of Varroa destructor (Acari: Varroidae) to synthetic acaricides in Uruguay: varroa mites’ potential to develop acaricide resistance. Parasitology Research 108, 215221. doi: 10.1007/s00436-010-2122-5.Google Scholar
Mishra, V. (2007). Oxidative stress and role of antioxidant supplementation in critical illness. Clinical Laboratory 53, 199209.Google Scholar
Murilhas, A. M. (2002). Varroa destructor infestation impact on Apis mellifera carnica capped worker brood production, bee population and honey storage in a Mediterranean climate. Apidologie 33, 271281. doi: 10.1051/apido:2002013.Google Scholar
Oakeshott, J. G., Johnson, R. M., Berebaum, M. R., Ranson, H., Cristino, A. S. and Claudianos, C. (2010). Metabolic enzymes associated with xenobiotic and chemosensory responses in Nesonia vitripennis . Insect Molecular Biology 19 (Suppl. 1), 147163. doi: 10.1111/j.1365-2583.2009.00961.x.Google Scholar
Papadopoulos, A. A., Polemitou, I., Yiangou, A. and Tananaki, C. (2004). Glutathione S-transferase in the developmental stages of the insect Apis mellifera macedonica . Comparative Biochemistry and Physiology C 139, 8792. doi: 10.1016/j.cca.2004.09.009.Google Scholar
Podczasy, J. J. and Wei, R. (1988). Reduction of iodonitrotetrazolium violet by superoxide radicals. Biochemical and Biophysical Research Communications 150, 12941301. doi: 10.1016/0006-291X(88)90770-X.Google Scholar
Rosenkranz, P., Aumeier, P. and Ziegelmann, B. (2010). Biology and control of Varroa destructor . Journal of Invertebrate Pathology 103 (Suppl.), S96S119. doi: 10.1016/j.jip.2009.07.016.Google Scholar
Sammataro, D., Gerson, U. and Needham, G. (2000). Parasitic mites of honey bees, life history, implications, and impact. Annual Review of Entomology 45, 519548.CrossRefGoogle ScholarPubMed
Sau, A., Pellizzari-Tregno, F., Valentino, F., Federici, G. and Cauccuri, A. M. (2010). Glutathione transferases and development of new principles to overcome drug resistance. Archives of Biochemistry and Biophysics 500, 116122. doi: 10.1016/j.abb.2010.05.012.Google Scholar
Sorci, G. and Faivre, B. (2009). Inflammation and oxidative stress in vertebrate host–parasite systems. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 7183. doi: 10.1098/rstb.2008.0151.Google Scholar
Stevenson, M. A., Benard, H., Bolger, P. and Morris, R. S. (2005). Spatial epidemiology of the Asian honey bee mite (Varroa destructor) in the North Island of New Zealand. Preventive Veterinary Medicine 71, 241252. doi: 10.1016/j.prevetmed.2005.07.007.Google Scholar
Van Engelsdorp, D., Evans, J. D., Saegerman, C., Mullin, Ch., Haubruge, E., Nguyen, B. K., Frazier, M., Frazier, J., Cox-Foster, D., Chen, Y., Underwood, R., Tarpy, D. R. and Pettis, J. S. (2009). Colony collapse disorder: a descriptive study. PLoS ONE 4, e 6481. doi: 10.1371/journal.pone.0006481.Google Scholar
Wilkinson, D. and Smith, G. C. (2002). A model of the mite parasite, Varroa destructor, on honeybees (Apis mellifera) to investigate parameters important to mite population growth. Ecological Modelling 148, 263275. doi: 10.1016/S0304-3800(01)00440-9.Google Scholar
Wu, J. Y., Anelli, C. M. and Sheppard, W. S. (2011). Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS ONE 6, e14720. doi: 10.1371/journal.pone.0014720.Google Scholar
Yang, X. and Cox-Foster, D. (2005). Impact of ectoparasite on the immunity and pathology of an invertebrate. Evidence for immunosuppression and viral amplification. Proceedings of the National Academy of Sciences USA 102, 74707475. doi: 10.1073/pnas.0501860102.Google Scholar
Żółtowska, K., Lipiński, Z. and Dmitryjuk, M. (2005). The total protein content, protein fractions and proteases activity of drone prepupae of Apis mellifera due to varroatosis. Wiadomości Parazytologiczne 51, 4347.Google Scholar