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Disease associations between honeybees and bumblebees as a threat to wild pollinators

Nature volume 506, pages 364–366 (2014)Cite this article

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Abstract

Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly1 and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops2. Honeybees (Apis mellifera), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high-impact pathogens3,4, and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumblebees (Bombus spp.) are in global decline5,6, one cause of which may be pathogen spillover from managed pollinators like honeybees7,8 or commercial colonies of bumblebees9. Here we use a combination of infection experiments and landscape-scale field data to show that honeybee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic parasite Nosema ceranae in honeybees and bumblebees is linked; as honeybees have higher DWV prevalence, and sympatric bumblebees and honeybees are infected by the same DWV strains, Apis is the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates10,11 highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators.

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Figure 1: DWV and N. ceranae infectivity in bumblebees.
Figure 2: Geographical distribution of DWV and N. ceranae across their pollinator hosts.
Figure 3: Sympatric Apis and Bombus share viral strains.

Accession codes

Accessions

GenBank/EMBL/DDBJ

Data deposits

Viral RNA sequences have been deposited in GenBank under accession numbers KF929216–KF929290.

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Acknowledgements

The authors are grateful to E. Fürst for technical support and R. J. Gill for discussions. We thank C. Jones, G. Baron and O. Ramos-Rodriguez for comments on previous versions of the manuscript. They also thank Hymettus Ltd for help with the field collections, K. Liu for help in the laboratory and B. McCrea and S. Baldwin for technical help in the bee laboratory. The study was supported by the Insect Pollinators Initiative (funded jointly by the Biotechnology and Biological Sciences Research Council, the Department for Environment, Food and Rural Affairs, the Natural Environment Research Council, The Scottish Government and The Wellcome Trust, under the Living with Environmental Change Partnership: grants BB/I000151/1 (M.J.F.B.), BB/I000100/1 (R.J.P.) and BB/I000097/1 (J.L.O.).

Author information

Authors and Affiliations

  1. Royal Holloway University of London, School of Biological Sciences, Bourne Building, Egham TW20 0EX, UK,

    M. A. Fürst & M. J. F. Brown

  2. IST Austria (Institute of Science and Technology Austria), 3400 Klosterneuburg, Austria,

    M. A. Fürst

  3. Queen's University Belfast, School of Biological Sciences, 97 Lisburn Road, Belfast BT9 7BL, UK,

    D. P. McMahon & R. J. Paxton

  4. Department of Agro-Ecology, Rothamsted Research, Harpenden AL5 2JQ, UK,

    J. L. Osborne

  5. University of Exeter, Environment & Sustainability Institute, Penryn TR10 9EZ, UK,

    J. L. Osborne

  6. Martin-Luther-Universität Halle-Wittenberg, Institute for Biology/General Zoology, Hoher Weg 8, 06120 Halle (Saale), Germany,

    R. J. Paxton

  7. German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany,

    R. J. Paxton

Authors
  1. M. A. Fürst
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  3. J. L. Osborne
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Contributions

The study was jointly conceived by R.J.P., J.L.O. and M.J.F.B. Experiments were designed by M.A.F. and M.J.F.B.; M.A.F prepared the manuscript; M.J.F.B., D.P.M., R.J.P. and J.L.O. edited the manuscript. M.A.F. carried out the experimental, molecular work and analyses, and D.P.M. undertook the phylogenetic analyses.

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Correspondence to M. A. Fürst.

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Extended data figures and tables

Extended Data Figure 1 Host bee species and sampling-site distributions.

Distribution of sampling sites across Great Britain and the Isle of Man. The most common Bombus species on a given site is represented by coloured letters and the second most common Bombus species is represented by the colours of the dots. Total sample sizes for each site are given in the table.

Extended Data Figure 2 Prevalence of DWV and N. ceranae per site and host bee species.

a–d, Pathogen prevalence in Bombus spp. in per cent per site for DWV (a) and for N. ceranae (b), and per species for DWV (c) and for N. ceranae (d). Bars indicate 95% confidence intervals. Note different scales.

Extended Data Figure 3 Raw data for prevalence of DVW and N. ceranae.

The linear models shown only illustrate the relationships but do not drive the conclusions in the main text. a, DWV presence in Apis and Bombus (adjusted R2 = 0.34, P < 0.001). b, DWV replicating in Bombus and DWV presence in Bombus (adjusted R2 = 0.46, P < 0.001). c, N. ceranae presence in Apis and Bombus (adjusted R2 = −0.04, P > 0.728). The line shows the best fit and the dark grey region shows 95% confidence interval of fit.

Extended Data Table 1 Pathogen prevalence per species
Full size table
Extended Data Table 2 Alternative models for the diversification of DWV and VDV viruses in UK pollinators
Full size table

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Fürst, M., McMahon, D., Osborne, J. et al. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–366 (2014). https://doi.org/10.1038/nature12977

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