Hyperthermia treatment can kill immature and adult Varroa destructor mites without reducing drone fertility

Abstract

In the last few decades, different hyperthermia devices have been developed to kill Varroa destructor mites in the colony. Intriguingly, effects of hyperthermia on Varroa destructor and honeybee brood have hardly been investigated. We exposed honeybee brood to temperatures of 41°C to 45°C to investigate effects on Varroa destructor in the hive and on drone fertility of treated colonies. Drone fertility is an important issue in keeping healthy and viable honeybee populations. We show that temperatures of 42°C for 3 hours or higher kill all the Varroa destructor but, unfortunately, also part of the honeybee brood. Temperatures below 42°C are ineffective against adult Varroa destructor. A temperature of 41°C and 2 hours duration is highly effective against immature Varroa destructor and thus interrupts their reproduction without harming the viability or fertility of drones, while longer durations or higher temperatures kill the spermatozoa of the drones.

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References

  1. Brodsgaard C.J., Hansen, H. (1994) An example of integrated biotechnical and soft chemical control of Varroa in a Danish apiary. In: Matheson A. (ed.): New Perspectives on Varroa, pp. 101–105.

  2. Büchler R., Berg S., Le Conte Y. (2010) Breeding for resistance to Varroa destructor in Europe, Apidologie 41, 393–408.

    Article  Google Scholar 

  3. Bolli H. K., Bogdanov S., Imdorf A., Fluri P. (1993) Action of formic acid on Varroa jacobsoni Oud. and the honeybee (Apis mellifera L), Apidologie 24, 1, 51–57.

    Article  Google Scholar 

  4. Bujok B., Kleinhenz M., Fuchs S., & Tautz J. (2002) Hot spots in the bee hive, Naturwissenschaften 89, 7, 299–301.

    CAS  Article  Google Scholar 

  5. Chen Y. P., Siede R. (2007) Honey bee viruses, Adv. Virus Res. 70, 33–80.

    CAS  Article  Google Scholar 

  6. Czekońska K., Chuda-Mickiewicz B., & Chorbiński P. (2013) The effect of brood incubation temperature on the reproductive value of honey bee (Apis mellifera) drones, J. Apic. Res. 52, 2, 96–105.

  7. Elzen P. J., Eischen F. A., Baxter J. B., Pettis J., Elzen G. W., Wilson W. T. (1998) Fluvalinate resistance in Varroa jacobsoni from several geographic locations, Am Bee J 138, 9, 674–676.

    Google Scholar 

  8. Engels W. (1998) Efficiency of Biotechnical Control of Varroasis by means of Hyperthermia, Apiacta 33, 2, 49–55.

    Google Scholar 

  9. Fahrbach S. E., Dobrin S. (2009) The How and Why of Structural Plasticity in the Adult Honeybee Brain, in: Dukas R., Ratcliffe J. M. (Ed.), Cognitive ecology II. University of Chicago Press, Chicago, pp. 27–46.

    Google Scholar 

  10. Fuchs S. (1990) Preference for drone brood cells by Varroa jacobsoni Oud in colonies of Apis mellifera carnica, Apidologie 21, 3, 193–199.

    Article  Google Scholar 

  11. Gallai N., Salles J.-M., Settele J., Vaissière B.E. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline, Ecol. Econ. 68, 3, 810–821.

    Article  Google Scholar 

  12. Goras G., Tananaki C.H., Gounari S., Dimou M., Lazaridou E., Karazafiris E., Kanelis D., Liolios V., El Taj H.F., Thrasyvoulou A. (2015) Hyperthermia -a non-chemical control strategy against Varroa, J Hell Vet Med Soc 66, 4, 249–256.

  13. Groh C., Tautz J., Rössler W. (2004) Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development, P Natl Acad Sci 101, 12, 4268–4273.

    CAS  Article  Google Scholar 

  14. Hoppe H., Ritter W. (1987) Experiments using combined heat therapy to control Varroa disease, Apidologie 18, 383–385.

    Google Scholar 

  15. Hourcade B., Muenz T.S., Sandoz J.-C., Rössler W., Devaud J.-M. (2010) Long-term memory leads to synaptic reorganization in the mushroom bodies. A memory trace in the insect brain?, J Neurosci 30, 18, 6461–6465.

    CAS  Article  Google Scholar 

  16. Huang Z. (2001) Mite zapper-a new and effective method for Varroa mite control, Am Bee J 141, 10, 730–732.

    Google Scholar 

  17. de Jong D., de Jong P.H., Goncalves L.S. (1982) Weight loss and other damage to developing worker honeybees from infestation with Varroa jacobsoni, J. Apic. Res. 21, 3, 165–167.

    Article  Google Scholar 

  18. Karpov B., Zabelin B. (1978) Heat treatment for the control of Varroa jacobsoni infestation in bees [in Russian], Veterinariya Moscow 5, 121–122.

    Google Scholar 

  19. Khrust I. I. (1978) Thermal treatment during Varroatosis [in Russian], Pchelovodstvo 6, 5–8.

    Google Scholar 

  20. Kleinhenz M., Bujok B., Fuchs S., & Tautz J. (2003) Hot bees in empty broodnest cells: heating from within, J. Exp. Biol. 206, 23, 4217–4231.

    Article  Google Scholar 

  21. Koeniger G., Ziegler-Himmelreich S., Koeniger N. (2006) Spermatozoa number of drones (Apis mellifera) depends on temperature during metamorphosis and sexual maturation, Apidologie 37, 620–621.

    Google Scholar 

  22. Komissar A.D. (1985) Heat-treatment of Varroa-infested honeybee colonies, Apiacta 20, 4, 113–117.

    Google Scholar 

  23. Le Conte Y., Arnold G., Desenfant P. (1990) Influence of brood temperature and hygrometry variations on the development of the honey bee ectoparasite Varroa jacobsoni (Mesostigmata: Varroidae), Environ. Entomol. 19, 6, 1780–1785.

    Article  Google Scholar 

  24. Le Conte Y., Mondet F. (2017): Natural Selection of Honeybees Against Varroa destructor, in: Vreeland R., Sammataro D. (Ed.), Beekeeping – From Science to Practice, Springer, Cham.

    Google Scholar 

  25. Machado I. C., Freitas B.M., Pereira J.O.P. (2004) Solitary bees. Conservation, rearing and management for pollination, Brazil. Universidade Federal do Ceará

  26. Muenz T. S., Groh C., Maisonnasse A., Le Conte Y., Plettner E., Rössler W. (2015) Neuronal plasticity in the mushroom body calyx during adult maturation in the honeybee and possible pheromonal influences, Dev Neurobiol 75, 12, 1368–1384.

    CAS  Article  Google Scholar 

  27. Peng Y.-S., Fang Y., Xu S., Ge L. (1987) The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite, Varroa jacobsoni Oudemans, J Invertebr Pathol 49, 1, 54–60.

    Article  Google Scholar 

  28. Pettis J.S., Rice N., Joselow K., vanEngelsdorp D., Chaimanee V. (2016) Colony failure linked to low sperm viability in honey bee (Apis mellifera) queens and an exploration of potential causative factors,Plos One 11.

  29. Ramsey S. D., Ochoa R., Bauchan G., Gulbronson C., Mowery J. D., Cohen A., Lim D. Joklik J., Cicero J. M., Ellis J. D., Hawthorne D., vanEngelsdorp D. (2019) Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph, PNAS 116, 5, 1792–1801.

    CAS  Article  Google Scholar 

  30. Rosenkranz P. (1987): Apidologie 18, 4, 385–388

  31. Rosenkranz P. (1988) Temperaturpräferenz der Varroa-Milbe und Stocktemperaturen in Bienenvölkern an Tropenstandorten (Acarina: Varroidae/Hymenoptera: Apidae), Entomologia Generalis 14, 2, 123–132.

    Article  Google Scholar 

  32. Rosenkranz P., Aumeier P., Ziegelmann B. (2010) Biology and control of Varroa destrutor, J. Invertebr. Pathol. 103, 96–119

    Article  Google Scholar 

  33. Ruttner H. (1977) Die Milbe Varroa jacobsoni Oudem., ein neuer Bienenparasit, J Pestic. Sci. 50, 11, 165–169.

    Google Scholar 

  34. Schneider P., Drescher W. (1987) The influence of Varroa jacobsoni Oud. on weight at emergence, development of weight and hypopharyngeal glands, and longevity of Apis mellifera L, Apidologie 18, 1, 101–110.

    Article  Google Scholar 

  35. Schulz A. E. (1984) Reproduktion und Populationsentwicklung der parasitischen Milbe Varroa jacobsoni Oud. in Abhängigkeit vom Brutzyklus ihres Wirtes Apis mellifera L. (I. TEIL), Apidologie 15, 4, 401–420.

    Article  Google Scholar 

  36. Soloveva L. F. (1983) Thermal treatment to control Varroa disease of honeybees [in Russian], Pchelovodstvo 1, 17–18.

    Google Scholar 

  37. Tarelho Z. (1981) Effects of low and high temperatures on the spermathogenesis of Apis mellifera L, Revista Brasilera de Genetica 4, 193–212.

    Google Scholar 

  38. Tautz J., Maier S., Groh C., Rössler W., Brockmann A. (2003) Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development, P Natl A Sci 100, 12, 7343–7347.

    CAS  Article  Google Scholar 

  39. VonPosern H. (1988) Stopping Varroa victory march, Am Bee Jo 128, 6, 425–428.

    Google Scholar 

  40. Wallner K. (1999) Varroacides and their residues in bee products, Apidologie 30, 2-3, 235–248.

    CAS  Article  Google Scholar 

  41. WHO (1999) WHO laboratory manual for the examination of human semen and sperm-cervical mucous interaction, Cambridge University Press.

  42. Williamson S.M., Baker D.D., Wright G.A. (2013) Acute exposure to a sublethal dosis of imidacloprid and coumaphos enhances olfactory learning and memory in the honeybee Apis mellifera, Invertebr. Neurosci. 13, 1, 63–70.

    CAS  Article  Google Scholar 

  43. Zanni V., Degirmenci L., Annoscia D., Scheiner R., Nazzi F. 2018 The reduced brood nursing by mite infested honey bees depends on their accelerated behavioral maturation, J. Insect Physiol. 109, 47–54.

    CAS  Article  Google Scholar 

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Acknowledgments

We like to thank all of the beekeepers at the Bavarian State Institute for Viticulture and Horticulture, Institute for Bee Research and Beekeeping for their great support and for providing us with the colonies.

Contributions

AK, SB, and SH conceived this research and designed experiments; RS participated in the interpretation of the data; AK performed experiments; AK and RS wrote the paper. All authors read the manuscript.

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Correspondence to Arne Kablau.

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Additional information

Le traitement par hyperthermie peut tuer les acariens Varroa destructor immatures et adultes sans réduire la fertilité des mâles.

Varroa destructor / Apis mellifera / température / viabilité du sperme.

Hyperthermie-Behandlungen können Entwicklungsstadien und adulte Milben von Varroa destructor töten ohne die Drohnenfertilität zu reduzieren.

Varroa destructor / Apis mellifera / Temperatur / Spermienvitalität.

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Kablau, A., Berg, S., Härtel, S. et al. Hyperthermia treatment can kill immature and adult Varroa destructor mites without reducing drone fertility. Apidologie 51, 307–315 (2020). https://doi.org/10.1007/s13592-019-00715-7

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Keywords

  • Varroa destructor
  • Apis mellifera
  • Temperature
  • Sperm viability