Skip to main content
Log in

The mating behavior of Varroa destructor is triggered by a female sex pheromone. Part 2: Identification and dose-dependent effects of components of the Varroa sex pheromone

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

Reproduction of female Varroa destructor happens within the sealed brood cell of the honeybee host. The mating represents the last step of the reproductive cycle and is usually performed between the mature male offspring and one or more daughter mites. By offering solvent extracts of freshly molted females to male Varroa mites in our mating bioassay, we could clearly confirm the presence of a volatile female sex pheromone. After separation of the extract into a polar and non-polar fraction, only the polar fraction elicited the typical mating behavior of male mites. GC-MS analysis of the active fraction revealed a pattern of three fatty acids as the main components and the respective ethyl esters. We could prove that all these substances stimulated the male mating behavior, and we present results on the dose-dependent reactions of the males toward these compounds. The identification of a Varroa sex pheromone might enable new options for a biological control of the parasite.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.

Similar content being viewed by others

References

  • Allan, S.A., Phillips, J.S., Taylor, D., Sonenshine, D.E. (1988) Genital sex pheromones of ixodid ticks: evidence for the role of fatty acids from the anterior reproductive tract in mating of Dermacentor variabilis and Dermacentor andersoni. J Insect Physiol 34(4), 315–323

    Article  CAS  Google Scholar 

  • Allan, S.A., Phillips, J.S., Sonenshine, D.E. (1991) Role of genital sex pheromones in Amblyomma americanum and A. maculatum (Acari: Ixodidae). Exp Appl Acarol 11, 9–21

    Article  PubMed  CAS  Google Scholar 

  • Chiroudi, E., Rosenkranz, P., Aumeier, P. (1997) Altersabhängige und rasenspezifische Duftstoffmuster bei Arbeiterinnen der Honigbiene (A. mellifera). Mittlg. der Ges. Allg Angew Entomol 11, 179–182

    Google Scholar 

  • Del Piccolo, F., Nazzi, F., Della, V.G., Milani, N. (2010) Selection of Apis mellifera workers by the parasitic mite Varroa destructor using host cuticular hydrocarbons. Parasitology 137, 967–973

    Article  PubMed  Google Scholar 

  • Donzé, G., Guerin, P.M. (1994) Behavioral attributes and parental care of Varroa mites parasitizing honeybee brood. Behav Ecol Sociobiol 34, 305–319

    Article  Google Scholar 

  • Donzé, G., Herrmann, M., Bachofen, B., Guerin, P.M. (1996) Effect of mating frequency and brood cell infestation rate on the reproductive success of the honeybee parasite Varroa jacobsoni. Ecol Entomol 21, 17–26

    Article  Google Scholar 

  • Garrido C. (2004) Reproduktionssteuerung bei der parasitischen Bienenmilbe Varroa destructor Anderson & Trueman (ehemals Varroa jacobsoni). Ph.D. Thesis at the Faculty of Biology at the University of Hohenheim, 82 pp.

  • Garrido, C., Rosenkranz, P. (2004) Volatiles of the honey bee larva initiate oogenesis in the parasitic mite Varroa destructor. Chemoecology 14, 193–197

    Google Scholar 

  • Kraus, B. (1993) Preferences of Varroa jacobsoni for honey bees Apis mellifera L. of different ages. J Apic Res 32, 57–64

    Google Scholar 

  • Kuenen, L.P.S., Calderone, N.W. (1997) Transfers of Varroa mites from newly emerged bee: preferences for age- and function-specific adult bees. J Insect Behav 10, 213–228

    Article  Google Scholar 

  • Le Conte, Y., Arnold, G. (1988) Etude du thermopreferendum de Varroa jacobsoni Oud. Apidologie 19, 155–164

    Article  Google Scholar 

  • Le Conte, Y., Arnold, G., Troullier, J., Masson, C., Chappe, B., Ourisson, G. (1989) Attraction of the parasitic mite Varroa to the drone larvae of honeybees by simple aliphatic esters. Science 245, 638–639

    Article  PubMed  Google Scholar 

  • Le Conte, Y., Arnold, G., Troullier, J., Masson, C., Chappe, B. (1990) Identification of a brood pheromone in honeybees. Naturwissenschaften 77, 334–336

    Article  Google Scholar 

  • Le Conte, Y., Streng, L., Troullier, J. (1994) The recognition of larvae by worker honeybees. Naturwissenschaften 81, 462–465

    Google Scholar 

  • Le Conte, Y., Mohammedi, A., Robinson, G.E. (2001) Primer effects of a brood pheromone on honeybee behavioural development. Proc R Soc London B 268, 163–168

    Article  Google Scholar 

  • Lindenmayer A. (2007) Chemotaktische Orientierung bei der Partnerfindung und Details des Kopulationsverhaltens der Bienenmilbe Varroa destructor, State Examination for Secondary School Teaching Qualification, Dept. of Biology, University of Tübingen.

  • Martin, C., Provost, E., Bagnères, A.G., Roux, M., Clèment, J.L., Le Conte, Y. (2002) Potential mechanism for detection by Apis mellifera of the parasitic mite Varroa destructor inside sealed brood cells. Physiol Entomol 27, 175–188

    Article  CAS  Google Scholar 

  • Milani, N., Chiesa, F. (1990) Some factors affecting the reproduction of Varroa jacobsoni Oud. under laboratory conditions. Apicoltura 6, 33–42

    Google Scholar 

  • Nation, J.L., Sanford, M.T., Milne, K. (1992) Cuticular hydrocarbons from Varroa jacobsoni. Exp Appl Acarol 16, 331–344

    Article  CAS  Google Scholar 

  • Nazzi, F., Milani, N., Della, V.G. (2004) A semiochemical from larval food influences the entrance of Varroa destructor into brood cells. Apidologie 35, 403–410

    Article  CAS  Google Scholar 

  • Nazzi, F., Bortolomeazzi, R., Della, V.G., Del Piccolo, F., Annoscia, D., Milani, N. (2009) Octanoic acid confers to royal jelly Varroa-repellent properties. Naturwissenschaften 96, 309–314

    Article  PubMed  CAS  Google Scholar 

  • Rickli, M., Guerin, P.M., Diehl, P.A. (1992) Palmitic acid released from honeybee worker larvae attracts the parasitic mite Varroa jacobsoni on a servosphere. Naturwissenschaften 79, 320–322

    Article  CAS  Google Scholar 

  • Rosenkranz, P. (1988) Temperaturpräferenz der Varroa-Milbe und Stocktemperaturen an Tropenstandorten. Entomol Gen 14, 123–132

    Google Scholar 

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

    Article  Google Scholar 

  • Schulz, S., Fuhlendorff, J., Steidle, J.L.M., Collatz, J., Franz, J.-T. (2004) Identification and biosynthesis of an aggregation pheromone of the storage mite Chortoglyphus arcuatus. ChemBioChem 5, 1500–1507

    Article  PubMed  CAS  Google Scholar 

  • Sonenshine, D.E. (2004) Pheromones and other semiochemicals of ticks and their use in tick control. Parasitology 129, 405–425

    Article  Google Scholar 

  • Stanley-Samuelson, D.W., Jurenka, R.A., Cripps, C., Blomquist, G.J., De Renobales, M. (1988) Fatty acids in insects: composition, metabolism, and biological significance. Arch. Insect Biochem. Physiol. 9(1), 1–33

    Article  CAS  Google Scholar 

  • Troullier, J., Arnold, G., Le Conte, Y., Masson, C., Chappe, B. (1991) Temporal pheromonal and kairomonal secretion in the brood of honeybees. Naturwissenschaften 78, 368–370

    Article  Google Scholar 

  • Troullier, J., Arnold, G., Chappe, B., Le Conte, Y., Masson, C. (1992) Semiochemical basis of infestation of honey bee brood by Varroa jacobsoni. J Chem Ecol 18(11), 2041–2053

    Article  Google Scholar 

  • Troullier, J., Milani, N. (1999) Stimulation of Varroa jacobsoni Oud. oviposition with semiochemicals from honeybee brood. Apidologie 30, 3–12

    Article  Google Scholar 

  • Witzgall, P., Stelinski, L., Gut, L., Thomson, D. (2008) Codling moth management and chemical ecology. Annu Rev Entomol 53, 503–522

    Article  PubMed  CAS  Google Scholar 

  • Wyatt, T.D. (1997) Putting pheromones to work: paths forward for direct control. In: Cardé, R.T., Minks, A.K. (eds.) Pheromone Research: New Directions, pp. 445–459. Chapman & Hall, New York

    Chapter  Google Scholar 

  • Wyatt, T.D. (2003) Pheromones and Animal Behavior: Communication by Smell and Taste. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Ziegelmann, B., Lindenmayer, A., Steidle, J., Rosenkranz, P. (2012) The mating behavior of Varroa destructor is triggered by a female sex pheromone, Part 1: Preference behavior of male mites in a laboratory bioassay. Apidologie. doi:10.1007/s13592-012-0182-5

Download references

Acknowledgments

We thank the Montagu Foundation and the Agroscope Liebefeld-Posieux for providing financial support. Dipl. Eng. Chem. Thomas Blum from the Department of Applied Chemistry of the University of Reutlingen performed the quantitative analysis. We are very grateful for his qualified support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bettina Ziegelmann.

Additional information

Manuscript editor: Yves Le Conte

Le comportement daccouplement de Varroa destructor est déclenché par une phéromone sexuelle de la femelle. Partie 2: Identification des composants de la phéromone sexuelle de Varroa et leurs effets en fonction de la dose

Acari / Varroa destructor / comportement daccouplement / pheromone sexuelle / Apidae

Das Paarungsverhalten von Varroa destructor wird durch ein weibliches Sexualpheromon gesteuert. Teil 2: Identifizierung und dosisabhängige Effekte von Komponenten des Varroa Sexualpheromons

Varroa destructor / Paarungsverhalten / Sexualpheromon

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ziegelmann, B., Tolasch, T., Steidle, J.L.M. et al. The mating behavior of Varroa destructor is triggered by a female sex pheromone. Part 2: Identification and dose-dependent effects of components of the Varroa sex pheromone. Apidologie 44, 481–490 (2013). https://doi.org/10.1007/s13592-013-0198-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-013-0198-5

Keywords

Navigation