IDEAS home Printed from https://ideas.repec.org/a/plo/ppat00/1004323.html
   My bibliography  Save this article

On the Front Line: Quantitative Virus Dynamics in Honeybee (Apis mellifera L.) Colonies along a New Expansion Front of the Parasite Varroa destructor

Author

Listed:
  • Fanny Mondet
  • Joachim R de Miranda
  • Andre Kretzschmar
  • Yves Le Conte
  • Alison R Mercer

Abstract

Over the past fifty years, annual honeybee (Apis mellifera) colony losses have been steadily increasing worldwide. These losses have occurred in parallel with the global spread of the honeybee parasite Varroa destructor. Indeed, Varroa mite infestations are considered to be a key explanatory factor for the widespread increase in annual honeybee colony mortality. The host-parasite relationship between honeybees and Varroa is complicated by the mite's close association with a range of honeybee viral pathogens. The 10-year history of the expanding front of Varroa infestation in New Zealand offered a rare opportunity to assess the dynamic quantitative and qualitative changes in honeybee viral landscapes in response to the arrival, spread and level of Varroa infestation. We studied the impact of de novo infestation of bee colonies by Varroa on the prevalence and titres of seven well-characterised honeybee viruses in both bees and mites, using a large-scale molecular ecology approach. We also examined the effect of the number of years since Varroa arrival on honeybee and mite viral titres. The dynamic shifts in the viral titres of black queen cell virus and Kashmir bee virus mirrored the patterns of change in Varroa infestation rates along the Varroa expansion front. The deformed wing virus (DWV) titres in bees continued to increase with Varroa infestation history, despite dropping infestation rates, which could be linked to increasing DWV titres in the mites. This suggests that the DWV titres in mites, perhaps boosted by virus replication, may be a major factor in maintaining the DWV epidemic after initial establishment. Both positive and negative associations were identified for several pairs of viruses, in response to the arrival of Varroa. These findings provide important new insights into the role of the parasitic mite Varroa destructor in influencing the viral landscape that affects honeybee colonies.Author Summary: Honeybees currently face a dramatic decline worldwide. The main honeybee parasite - Varroa destructor - plays a key role in these mortalities, since uncontrolled infestation inevitably results in the death of the colony. The pathological effects of Varroa infestations are partly attributed to the association of the mite with several honeybee viruses, primarily deformed wing virus (DWV). However the exact role that Varroa plays in the spread of honeybee viruses is still unknown. The recent arrival of Varroa in New Zealand provided a timely opportunity to gain insights into the complex relationship between bees, Varroa and viruses. Our data reveal that the different viruses have unique quantitative dynamics in relation to Varroa infestation, resulting in a shifting succession of virus infections that ultimately leaves DWV as the predominant infection. Assumption-free analysis shows consistent clustering of the data according to Varroa-infestation history, confirming a progressive change in the overall virus landscape co-incident with Varroa infestation. We also highlight possible interactions between several viruses. Our findings may have implications for the beekeeping industry, by highlighting the dynamic changes in the virus infections due to the arrival of Varroa, and how these are maintained.

Suggested Citation

  • Fanny Mondet & Joachim R de Miranda & Andre Kretzschmar & Yves Le Conte & Alison R Mercer, 2014. "On the Front Line: Quantitative Virus Dynamics in Honeybee (Apis mellifera L.) Colonies along a New Expansion Front of the Parasite Varroa destructor," PLOS Pathogens, Public Library of Science, vol. 10(8), pages 1-15, August.
  • Handle: RePEc:plo:ppat00:1004323
    DOI: 10.1371/journal.ppat.1004323
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1004323
    Download Restriction: no

    File URL: https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1004323&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.ppat.1004323?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Merav Gleit Kielmanowicz & Alex Inberg & Inbar Maayan Lerner & Yael Golani & Nicholas Brown & Catherine Louise Turner & Gerald J R Hayes & Joan M Ballam, 2015. "Prospective Large-Scale Field Study Generates Predictive Model Identifying Major Contributors to Colony Losses," PLOS Pathogens, Public Library of Science, vol. 11(4), pages 1-20, April.
    2. Monica Vercelli & Luca Croce & Teresina Mancuso, 2020. "An Economic Approach to Assess the Annual Stock in Beekeeping Farms: The Honey Bee Colony Inventory Tool," Sustainability, MDPI, vol. 12(21), pages 1-14, November.
    3. Teresina Mancuso & Luca Croce & Monica Vercelli, 2020. "Total Brood Removal and Other Biotechniques for the Sustainable Control of Varroa Mites in Honey Bee Colonies: Economic Impact in Beekeeping Farm Case Studies in Northwestern Italy," Sustainability, MDPI, vol. 12(6), pages 1-16, March.
    4. Dimitri Breda & Davide Frizzera & Giulia Giordano & Elisa Seffin & Virginia Zanni & Desiderato Annoscia & Christopher J. Topping & Franco Blanchini & Francesco Nazzi, 2022. "A deeper understanding of system interactions can explain contradictory field results on pesticide impact on honey bees," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:ppat00:1004323. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    We have no bibliographic references for this item. You can help adding them by using this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plospathogens (email available below). General contact details of provider: https://journals.plos.org/plospathogens .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.