Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-26T13:17:35.640Z Has data issue: false hasContentIssue false
  • English
  • Français

Resistance rather than tolerance explains survival of savannah honeybees (Apis mellifera scutellata) to infestation by the parasitic mite Varroa destructor

Published online by Cambridge University Press:  22 December 2015

URSULA STRAUSS ,
VINCENT DIETEMANN ,
HANNELIE HUMAN ,
ROBIN M. CREWE  and
CHRISTIAN W. W. PIRK
URSULA STRAUSS
Affiliation:
Department of Zoology and Entomology, Social Insect Research Group, University of Pretoria, Private Bag X20, Hatfield, Pretoria 0028, South Africa
VINCENT DIETEMANN
Affiliation:
Department of Zoology and Entomology, Social Insect Research Group, University of Pretoria, Private Bag X20, Hatfield, Pretoria 0028, South Africa Agroscope, Swiss Bee Research Centre, 3003 Bern, Switzerland
HANNELIE HUMAN
Affiliation:
Department of Zoology and Entomology, Social Insect Research Group, University of Pretoria, Private Bag X20, Hatfield, Pretoria 0028, South Africa
ROBIN M. CREWE
Affiliation:
Department of Zoology and Entomology, Social Insect Research Group, University of Pretoria, Private Bag X20, Hatfield, Pretoria 0028, South Africa
CHRISTIAN W. W. PIRK*
Affiliation:
Department of Zoology and Entomology, Social Insect Research Group, University of Pretoria, Private Bag X20, Hatfield, Pretoria 0028, South Africa
*
*Corresponding author: Department of Zoology and Entomology, Social Insect Research Group, University of Pretoria, Private Bag X20, Hatfield, Pretoria 0028, South Africa. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Varroa destructor is considered the most damaging parasite affecting honeybees (Apis mellifera L.). However, some honeybee populations such as the savannah honeybee (Apis mellifera scutellata) can survive mite infestation without treatment. It is unclear if survival is due to resistance mechanisms decreasing parasite reproduction or to tolerance mechanisms decreasing the detrimental effects of mites on the host. This study investigates both aspects by quantifying the reproductive output of V. destructor and its physiological costs at the individual host level. Costs measured were not consistently lower when compared with susceptible honeybee populations, indicating a lack of tolerance. In contrast, reproduction of V. destructor mites was distinctly lower than in susceptible populations. There was higher proportion of infertile individuals and the reproductive success of fertile mites was lower than measured to date, even in surviving populations. Our results suggest that survival of savannah honeybees is based on resistance rather than tolerance to this parasite. We identified traits that may be useful for breeding programmes aimed at increasing the survival of susceptible populations. African honeybees may have benefited from a lack of human interference, allowing natural selection to shape a population of honeybees that is more resistant to Varroa mite infestation.

Keywords

Apis mellifera scutellataVarroa destructorresistancetolerancephysiological costmitereproduction
Type
Research Article
Information
Parasitology , Volume 143 , Issue 3 , March 2016 , pp. 374 - 387
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

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

Abel, S., Abel zur Wiesch, P., Davis, B. M. and Waldor, M. K. (2015). Analysis of bottlenecks in experimental models of infection. PLoS Pathogens 11, e1004823.CrossRefGoogle ScholarPubMed
Alaux, C., Dantec, C., Parrinello, H. and Le Conte, Y. (2011). Nutrigenomics in honey bees: digital gene expression analysis of pollen's nutritive effects on healthy and varroa-parasitized bees. Genomics 12, 496.Google Scholar
Allsopp, M. H. (1997). Varroa jacobsoni in South Africa. South African Bee Journal 69, 73–82.Google Scholar
Allsopp, M. H. (2006). Analysis of Varroa destructor infestation of southern African honeybee populations. M.Sc. thesis, University of Pretoria, Pretoria, South Africa.Google Scholar
Amdam, G. V., Hartfelder, K., Norberg, K., Hagen, A. and Omholt, S. W. (2004). Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): a factor in colony loss during overwintering? Journal of Economic Entomology 97, 741–747.Google Scholar
Annoscia, D., Del Piccolo, F. and Nazzi, F. (2012). How does the mite Varroa destructor kill the honeybee Apis mellifera? Alteration of cuticular hydrocarbons and water loss in infested honeybees. Journal of Insect Physiology 58, 1548–1555.Google Scholar
Aronstein, K. A., Saldivar, E., Vega, R., Westmiller, S. and Douglas, A. E. (2012). How Varroa parasitism affects the immunological and nutritional status of the honey bee, Apis mellifera . Insects 3, 601–615.Google Scholar
Boot, W. J., Schoenmaker, J., Calis, J. N. M. and Beetsma, J. (1995 a ). Invasion of Varroa jacobsoni into drone brood cells of the honey bee. Apis mellifera . Apidologie 26, 109–118.CrossRefGoogle Scholar
Boot, W. J., van Baalen, M. and Sabelis, M. W. (1995 b). Why do Varroa mites invade worker brood cells of the honey bee despite lower reproductive success? Behavioral Ecology and Sociobiology 36, 283–289.CrossRefGoogle Scholar
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, 207–217.Google Scholar
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Calderón, R. A., Ureña, S. and van Veen, J. W. (2012). Reproduction of Varroa destructor and offspring mortality in worker and drone brood cells of Africanized honey bees. Experimental and Applied Acarology 56, 297–307.CrossRefGoogle ScholarPubMed
Carneiro, F. E., Torres, R. R., Strapazzon, R., Ramirez, S. A., Guerra, J. C. V., Koling, D. F. and Moretto, G. (2007). Changes in the reproductive ability of the mite Varroa destructor (Anderson and Trueman) in Africanized honey bees (Apis mellifera L.) (Hymenoptera: Apidae) colonies in southern Brazil. Neotropical Entomology 36, 949–952.Google Scholar
Contzen, C., Garedew, A., Lamprecht, I. and Schmolz, E. (2004). Calorimetrical and biochemical investigations on the influence of the parasitic mite Varroa destructor on the development of honeybee brood. Thermochimica Acta 415, 115–121.Google Scholar
De Jong, D. and De Jong, P. H. (1983). Longevity of Africanized honey bees (Hymenoptera: Apidae) infested by Varroa jacobsoni (Parasitiformes: Varroidae). Journal of Economic Entomology 76, 766–768.Google Scholar
De Jong, D. and Soares, A. E. E. (1997). An isolated population of Italian bees that has survived Varroa jacobsoni infestation without treatment for over 12 years. American Bee Journal 137, 742–747.Google Scholar
De Jong, D., De Jong, P. H. and Gonçalves, L. S. (1982). Weight loss and other damage to developing worker honeybees from infestation with Varroa jacobsoni . Journal of Apicultural Research 21, 165–167.Google Scholar
de Miranda, J. R. and Genersch, E. (2010). Deformed wing virus. Journal of Invertebrate Pathology 103, 48–61.Google Scholar
de Miranda, J. R., Bailey, L., Ball, B. V., Blanchard, P., Budge, G. E., Chejanovsky, N., Chen, Y-P., Gauthier, L., Genersch, E., de Graaf, D. C., Ribière, M., Ryabov, E., De Smet, L. and van der Steen, J. J. M. (2013). Standard methods for virus research in Apis mellifera . In The COLOSS BEEBOOK, Volume II: Standard Methods for Apis mellifera Pest and Pathogen Research (ed. Dietemann, V., Ellis, J. D. and Neumann, P.). Journal of Apicultural Research 52, doi: 10.3896/IBRA.1.52.4.22.Google Scholar
Dietemann, V., Pirk, C. W. W. and Crewe, R. M. (2009). Is there a need for conservation of honeybees in Africa? Apidologie 40, 285–295.Google Scholar
Dietemann, V., Pflugfelder, J., Anderson, D., Charrière, J. D., Chejanovsky, N., Dainat, B., de Miranda, J. R., Delaplane, K., Dillier, F. X., Fuchs, S., Gallmann, P., Gauthier, L., Imdorf, A., Koeniger, N., Kralj, J., Meikle, W., Pettis, J., Rosenkranz, P., Sammataro, D., Smith, D., Yañez, O. and Neumann, P. (2012). Varroa destructor: research avenues towards sustainable control. Journal of Apicultural Research 51, 125–132.Google Scholar
Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D. L., Locke, B., Delaplane, K. S., Wauquiez, Q., Tannahill, C., Frey, E., Ziegelmann, B., Rosenkranz, P. and Ellis, J. D. (2013). Standard methods for varroa research. In The COLOSS BEEBOOK, Volume II: Standard Methods for Apis mellifera Pest and Pathogen Research (ed. Dietemann, V., Ellis, J. D. and Neumann, P.). Journal of Apicultural Research 52, doi: 10.3896/IBRA.1.52.1.09.Google Scholar
Donzé, G. and Guerin, P. M. (1994). Behavioral attributes and parental care of Varroa mites parasitizing honeybee brood. Behavioral Ecology and Sociobiology 34, 305–319.Google Scholar
Donzé, G., Herrmann, M., Bachofen, B. and Guerin, P. M. (1996). Effect of mating frequency and brood cell infestation rate on the reproductive success of the honeybee parasite Varroa jacobsoni . Ecological Entomology 21, 17–26.Google Scholar
Duay, P. (2002). Relation between the level of preimaginal infestation by the brood mite Varroa destructor and adult life expectancy in drone honeybees (Hymenoptera: Apidae: Apis mellifera). Entomologia Generalis 26, 213–218.Google Scholar
Duay, P., De Jong, D. and Engels, W. (2002). Decreased flight performance and sperm production in drones of the honey bee (Apis mellifera) slightly infested by Varroa destructor mites during pupal development. Genetics and Molecular Research 1, 227–232.Google ScholarPubMed
Duay, P., De Jong, D. and Engels, W. (2003). Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites. Apidologie 34, 61–65.Google Scholar
Eguaras, M., Marcangeli, J. and Fernandez, N. A. (1994). Influence of ‘parasitic intensity’ on Varroa jacobsoni Oud reproduction. Journal of Apicultural Research 33, 155–159.Google Scholar
Fletcher, D. J. C. (1978). The African bee, Apis mellifera adansonii, in Africa. Annual Review of Entomology 23, 151–171.Google Scholar
Frey, E., Odemer, R., Blum, T. and Rosenkranz, P. (2013). Activation and interruption of the reproduction of Varroa destructor is triggered by host signals (Apis mellifera). Journal of Invertebrate Pathology 113, 56–62.Google Scholar
Fries, I., Camazine, S. and Sneyd, J. (1994). Population dynamics of Varroa jacobsoni: a model and a review. Bee World 75, 5–28.Google Scholar
Fries, I., Imdorf, A. and Rosenkranz, P. (2006). Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie 37, 564–570.Google Scholar
Fuchs, S. (1990). Preference for drone brood cells by Varroa jacobsoni Oud in colonies of Apis mellifera carnica . Apidologie 21, 193–199.CrossRefGoogle Scholar
Fuchs, S. and Langenbach, K. (1989). Multiple infestation of Apis mellifera L. brood cells and reproduction in Varroa jacobsoni Oud. Apidologie 20, 257–266.CrossRefGoogle Scholar
Garrido, C. and Rosenkranz, P. (2004). Volatiles of the honey bee larva initiate oogenesis in the parasitic mite Varroa destructor . Chemoecology 14, 193–197.Google Scholar
Garrido, C., Rosenkranz, P., Paxton, R. J. and Gonçalves, L. S. (2003). Temporal changes in Varroa destructor fertility and haplotype in Brazil. Apidologie 34, 535–541.Google Scholar
Gisder, S., Aumeier, P. and Genersch, E. (2009). Deformed wing virus (DWV): viral load and replication in mites (Varroa destructor). Journal of General Virology 90, 463–467.Google Scholar
Glinski, Z. and Jarosz, J. (1984). Alterations in haemolymph proteins of drone honey bee larvae parasitised by Varroa jacobsoni . Apidologie 15, 329–338.Google Scholar
Glinski, Z. and Jarosz, J. (1992). Varroa jacobsoni as a carrier of bacterial infections to a recipient bee host. Apidologie 23, 25–31.CrossRefGoogle Scholar
Harbo, J. R. and Harris, J. W. (2005). Suppressed mite reproduction explained by the behaviour of adult bees. Journal of Apicultural Research 44, 21–23.Google Scholar
Harris, J. W., Danka, R. G. and Villa, J. D. (2010). Honey bees (Hymenoptera: Apidae) with the trait of varroa sensitive hygiene remove brood with all reproductive stages of varroa mites (Mesostigmata: Varroidae). Annals of the Entomological Society of America 103, 146–152.Google Scholar
Hrassnigg, N. and Crailsheim, K. (2005). Differences in drone and worker physiology in honeybees. Apidologie 36, 255–277.Google Scholar
Human, H., Archer, C. R., du Rand, E. E., Pirk, C. W. W. and Nicolson, S. W. (2014). Resistance of developing honeybee larvae during chronic exposure to dietary nicotine. Journal of Insect Physiology 69, 74–79.Google Scholar
Jandricic, S. E. and Otis, G. W. (2003). The potential for using male selection in breeding honey bees resistant to Varroa destructor . Bee World 84, 155–164.Google Scholar
Jarolimek, J. P. and Otis, G. W. (2001). A comparison of fitness components in large and small honeybee drones. American Bee Journal 12, 891–892.Google Scholar
Kefuss, J., Vanpouke, J., De Lahitte, J. D. and Ritter, W. (2004). Varroa tolerance in France of Intermissa bees from Tunisia and their naturally mated descendants: 1993–2004. American Bee Journal 144, 563–568.Google Scholar
Kirrane, M. J., de Guzman, L. I., Rinderer, T. E., Frake, A. M., Wagnitz, J. and Whelan, P. M. (2011). Asynchronous development of honey bee host and Varroa destructor (Mesostigmata: Varroidae) influences reproductive potential of mites. Journal of Economic Entomology 104, 1146–1152.Google Scholar
Kralj, J. and Fuchs, S. (2006). Parasitic Varroa destructor mites influence flight duration and homing ability of infested Apis mellifera foragers. Apidologie 37, 577–587.Google Scholar
Kuster, R. D., Boncristiani, H. F. and Rueppell, O. (2014). Immunogene and viral transcript dynamics during parasitic Varroa destructor mite infection of developing honey bee (Apis mellifera) pupae. Journal of Experimental Biology 217, 1710–1718.Google Scholar
Le Conte, Y., de Vaublanc, G., Crauser, D., Jeanne, F., Rousselle, J-C. and Bécard, J-M. (2007). Honey bee colonies that have survived Varroa destructor . Apidologie 38, 566–572.CrossRefGoogle Scholar
Liu, T. (1996). Varroa mites as carriers of honey bee Chalkbrood. American Bee Journal 136, 655.Google Scholar
Locke, B. and Fries, I. (2011). Characteristics of honey bee colonies (Apis mellifera) in Sweden surviving Varroa destructor infestation. Apidologie 42, 533–542.Google Scholar
Locke, B., Le Conte, Y., Crauser, D. and Fries, I. (2012). Host adaptations reduce the reproductive success of Varroa destructor in two distinct European honey bee populations. Ecology and Evolution 2, 1144–1150.CrossRefGoogle ScholarPubMed
Marcangeli, J., Monetti, L. and Fernandez, N. (1992). Malformations produced by V. jacobsoni on Apis mellifera in the province of Buenos Aires, Argentina. Apidologie 23, 399–402.Google Scholar
Martin, S. J. (1994). Ontogenesis of the mite Varroa jacobsoni Oud. in worker brood of the honeybee Apis mellifera L. under natural conditions. Experimental and Applied Acarology 18, 87–100.Google Scholar
Martin, S. J. (1995 a). Ontogenesis of the mite Varroa jacobsoni Oud. in drone brood of the honeybee Apis mellifera L. under natural conditions. Experimental and Applied Acarology 19, 199–210.Google Scholar
Martin, S. J. (1995 b). Reproduction of Varroa jacobsoni in cells of Apis mellifera containing one or more mother mites and the distribution of these cells. Journal of Apicultural Research 34, 187–196.Google Scholar
Martin, S. J. (2001). Varroa destructor reproduction during the winter in Apis mellifera colonies in UK. Experimental and Applied Acarology 25, 321–325.Google Scholar
Martin, S. J. and Kryger, P. (2002). Reproduction of Varroa destructor in South African honey bees: does cell space influence Varroa male survivorship? Apidologie 33, 51–61.Google Scholar
Martin, S. J., Holland, K. and Murray, M. (1997). Non-reproduction in the honeybee mite Varroa jacobsoni . Experimental and Applied Acarology 21, 539–549.Google Scholar
McMenamin, A. J. and Genersch, E. (2015). Honey bee colony losses and associated viruses. Current Opinion in Insect Science 8, 121–129.Google Scholar
Medina, L. M. and Martin, S. J. (1999). A comparative study of Varroa jacobsoni reproduction in worker cells of honey bees (Apis mellifera) in England and Africanized bees in Yucatan, Mexico. Experimental and Applied Acarology 23, 659–667.Google Scholar
Milani, N., Della Vedova, G. and Nazzi, F. (2004). (Z)-8-Heptadecene reduces the reproduction of Varroa destructor in brood cells. Apidologie 35, 265–273.Google Scholar
Mondragón, L., Martin, S. J. and Vandame, R. (2006). Mortality of mite offspring: a major component of Varroa destructor resistance in a population of Africanized bees. Apidologie 37, 67–74.Google Scholar
Moritz, R. F. A. (1985). Heritability of the postcapping stage in Apis mellifera and its relation to varroatosis resistance. Journal of Heredity 76, 267–270.Google Scholar
Moritz, R. F. A. and Mautz, D. (1990). Development of Varroa jacobsoni in colonies of Apis mellifera capensis and Apis mellifera carnica . Apidologie 21, 53–58.Google Scholar
Pinto, F. A., Souza, G. K., Sanches, M. A. and Serrão, J. E. (2011). Parasitic effects of Varroa destructor (Acari: Varroidae) on hypopharyngeal glands of Africanized Apis mellifera (Hymenoptera: Apidae). Sociobiology 58, 769–778.Google Scholar
Pirk, C. W. W., Human, H., Crewe, R. M. and vanEngelsdorp, D. (2014). A survey of managed honey bee colony losses in the Republic of South Africa – 2009 to 2011. Journal of Apicultural Research 53, 35–42.Google Scholar
Råberg, L., Sim, D. and Read, A. F. (2007). Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318, 812–814.Google Scholar
Råberg, L., Graham, A. L. and Read, A. F. (2009). Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 37–49.Google Scholar
Ritter, W. (1993). New results of the development of tolerance to Varroa jacobsoni in bee colonies in Tunisia. In Asian Apiculture (ed. Connor, L. J., Rinderer, T. E., Sylvester, H. A. and Wongsiri, S.), pp. 463–467. Wicwas Press, Cheshire, USA.Google Scholar
Rosenkranz, P. (1999). Honey bee (Apis mellifera L.) tolerance to Varroa jacobsoni Oud. in South America. Apidologie 30, 159–172.Google Scholar
Rosenkranz, P. and Engels, W. (1994). Infertility of Varroa jacobsoni females after invasion into Apis mellifera worker brood as a tolerance factor against varroatosis. Apidologie 25, 402–411.Google Scholar
Rosenkranz, P., Aumeier, P. and Ziegelmann, B. (2010). Biology and control of Varroa destructor . Journal of Invertebrate Pathology 103, 96–119.Google Scholar
Ruttner, F. and Marx, G. (1984). Observation about a possible adaptation of Varroa jacobsoni to Apis mellifera L. in Uruguay. Apidologie 15, 43–62.Google Scholar
Schlüns, H., Schlüns, E. A., van Praagh, J. and Moritz, R. F. A. (2003). Sperm numbers in drone honeybees (Apis mellifera) depend on body size. Apidologie 34, 577–584.Google Scholar
Schneider, P. and Drescher, W. (1987). Einfluss der Parasitierung durch die Milbe Varroa jacobsoni Oud auf das Schlupfgewicht, die Gewichtsentwicklung, die Entwicklung der Hypopharynxdrüsen und die Lebensdauer von Apis mellifera L. Apidologie 18, 101–110.Google Scholar
Seeley, T. D. (2007). Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States. Apidologie 38, 19–29.Google Scholar
Seeley, T. D., Tarpy, D. R., Griffin, S. R., Carcione, A. and Delaney, D. A. (2015). A survivor population of wild colonies of European honeybees in the northeastern United States: investigating its genetic structure. Apidologie 46, 654–666. doi: 10.1007/s13592-015-0355-0.Google Scholar
Strauss, U., Human, H., Gauthier, L., Crewe, R. M., Dietemann, V. and Pirk, C. W. W. (2013). Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata). Journal of Invertebrate Pathology 114, 45–52.Google Scholar
Strauss, U., Pirk, C. W. W., Crewe, R. M., Human, H. and Dietemann, V. (2015). Impact of Varroa destructor on honeybee (Apis mellifera scutellata) colony development in South Africa. Experimental and Applied Acarology 65, 89–106.Google Scholar
Strick, H. and Madel, G. (1988). Transmission of the pathogenic bacterium Hafnia alvei to honey bees by the ectoparasitic mite Varroa jacobsoni . In Africanized Honey Bees and Bee Mites (ed. Needham, G. R., Page, R. E., Delfinado-Baker, M. and Bowman, C. E.), pp. 462–466. Ellis Horwood Limited, Chichester, UK.Google Scholar
Tribe, G. D. and Allsopp, M. H. (2001). Life history of the honeybee colony. In Beekeeping in South Africa (ed. Johannsmeier, M. F.), pp. 17–26. Plant Protection Handbook No. 14, Agricultural Research Council, Pretoria.Google Scholar
van Dooremalen, C., Gerritsen, L., Cornelissen, B., van der Steen, J. J. M., van Langevelde, F. and Blacquière, T. (2012). Winter survival of individual honey bees and honey bee colonies depends on level of Varroa destructor infestation. PLoS ONE 7, e36285.Google Scholar
van Dooremalen, C., Stam, E., Gerritsen, L., Cornelissen, B., van der Steen, J. J. M., van Langevelde, F. and Blacquière, T. (2013). Interactive effect of reduced pollen availability and Varroa destructor infestation limits growth and protein content of young honey bees. Journal of Insect Physiology 59, 487–493.Google Scholar
Wallberg, A., Han, F., Wellhagen, G., Dahle, B., Kawata, M., Haddad, N., Simões, Z. L. P., Allsopp, M. H., Kandemir, I., De la Rúa, P., Pirk, C. W. W. and Webster, M. T. (2014). A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera . Nature Genetics 46, 1081–1088.Google Scholar
Weinberg, K. P. and Madel, G. (1985). The influence of the mite Varroa jacobsoni Oud. on the protein concentration and the haemolymph volume of the brood of worker bees and drones of the honey bee Apis mellifera L. Apidologie 16, 421–436.Google Scholar
Wendling, S., Guillet, B., Roy, L., Kreiter, S. and Colin, M-E. (2014). Fertilization and fertility in the female of Varroa destructor, a key point for the parasite population dynamics. Apidologie 45, 722–732.Google Scholar
Yang, X. and Cox-Foster, D. (2007). Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology 134, 405–412.Google Scholar
Zioni, N., Soroker, V. and Chejanovsky, N. (2011). Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1-deformed wing virus recombinant (VDV-1-DWV) in the head of the honey bee. Virology 417, 106–112.Google Scholar
Żółtowska, K., Lipiński, Z. and Dmitryjuk, M. (2005). The total protein content, protein fractions and proteases activities of drone prepupae of Apis mellifera due to varrosis. Wiadomooeci Parazytologiczne 51, 39–43.Google ScholarPubMed