Advertisement

Ambio

, Volume 44, Issue 7, pp 694–704 | Cite as

The New Zealand experience of varroa invasion highlights research opportunities for Australia

  • Jay M. Iwasaki
  • Barbara I. P. Barratt
  • Janice M. Lord
  • Alison R. Mercer
  • Katharine J. M. Dickinson
Perspective

Abstract

The Varroa mite (Varroa destructor) is implicated as a major disease factor in honey bee (Apis mellifera) populations worldwide. Honey bees are extensively relied upon for pollination services, and in countries such as New Zealand and Australia where honey bees have been introduced specifically for commercial pollinator services, the economic effects of any decline in honey bee numbers are predicted to be profound. V. destructor established in New Zealand in 2000 but as yet, Australia remains Varroa-free. Here we analyze the history of V. destructor invasion and spread in New Zealand and discuss the likely long-term impacts. When the mite was discovered in New Zealand, it was considered too well established for eradication to be feasible. Despite control efforts, V. destructor has since spread throughout the country. Today, assessing the impacts of the arrival of V. destructor in this country is compromised by a paucity of data on pollinator communities as they existed prior to invasion. Australia’s Varroa-free status provides a rare and likely brief window of opportunity for the global bee research community to gain understanding of honey bee-native pollinator community dynamics prior to Varroa invasion.

Keywords

Apis mellifera Bombus Deformed wing virus Pollinator communities Varroa destructor 

Notes

Acknowledgments

We would like to thank several anonymous reviewers for input on an earlier version of this manuscript. We would also like to thank Ken Miller for help with Figure design, as well as Alexander Wild, for allowing use of his images in journal articles free of license fees.

References

  1. Barnett, J., and J. Pauling. 2005. The environmental effects of New Zealand’s free-market reforms. Environment, Development and Sustainability 7: 271–289. doi: 10.1007/s10668-005-7316-0.CrossRefGoogle Scholar
  2. Barry, S., D. Cook, R. Duthie, D. Clifford, and D. Anderson. 2010. Future Surveillance Needs for Honeybee Biosecurity. Rural Industries Research and Development Corporation 10/107.Google Scholar
  3. Batley, M., and K. Hogendoorn. 2009. Diversity and conservation status of native Australian bees. Apidologie 40: 347–354. doi: 10.1051/apido/2009018.CrossRefGoogle Scholar
  4. Benard, H., P. Bolger, M. Stone, and R. Thornton. 2001. The outbreak of Varroa destructor in New Zealand bees: Delimiting survey results and management options. Surveillance 28: 3–5.Google Scholar
  5. Bischoff, M., D.R. Campbell, J.M. Lord, and A.W. Robertson. 2013. The relative importance of solitary bees and syrphid flies as pollinators of two outcrossing plant species in the New Zealand alpine. Austral Ecology 38: 169–176. doi: 10.1111/j.1442-9993.2012.02389.x.CrossRefGoogle Scholar
  6. Blanche, K.R., J.A. Ludwig, and S.A. Cunningham. 2006. Proximity to rainforest enhances pollination and fruit set in orchards. Journal of Applied Ecology 43: 1182–1187. doi: 10.1111/j.1365-2664.2006.01230.x.CrossRefGoogle Scholar
  7. Campbell, D.R., M. Bischoff, J.M. Lord, and A.W. Robertson. 2010. Flower color influences insect visitation in alpine New Zealand. Ecology 91: 2638–2649.CrossRefGoogle Scholar
  8. Carvell, C. 2002. Habitat use and conservation of bumblebees (Bombus spp.) under different grassland management regimes. Biological Conservation 103: 33–49. doi: 10.1016/S0006-3207(01)00114-8.CrossRefGoogle Scholar
  9. Le Conte, Y., G. de Vaublanc, D. Crauser, F. Jeanne, J.-C. Rousselle, and J.-M. Bécard. 2007. Honey bee colonies that have survived Varroa destructor. Apidologie 38: 566–572. doi: 10.1051/apido:2007040.CrossRefGoogle Scholar
  10. CSIRO. 2014. Australia’s biosecurity future: Preparing for future biological challenges. Canberra: CSIRO.Google Scholar
  11. Cunningham, S.A., F. FitzGibbon, and T. Heard. 2002. The future of pollinators for Australian agriculture. Australian Journal of Agricultural Research 53: 893–900.CrossRefGoogle Scholar
  12. Cunningham, S.A., N.A. Schellhorn, A. Marcora, and M. Batley. 2013. Movement and phenology of bees in a subtropical Australian agricultural landscape. Austral Ecology 38: 456–464. doi: 10.1111/j.1442-9993.2012.02432.x.CrossRefGoogle Scholar
  13. Department of Agriculture, Fisheries, and Forestry. 2011. A honey bee industry and pollination continuity strategy should Varroa become established in Australia. Auckland: Australian Government.Google Scholar
  14. Donovan, B.J. 1980. Interactions between native and introduced bees in New Zealand. New Zealand Journal of Ecology 3: 104–116.Google Scholar
  15. Donovan, B. J. 2007. Apoidea (Insecta: Hymenoptera). In Fauna of New Zealand 57. Landcare Research.Google Scholar
  16. Fürst, M.A., D.P. McMahon, J.L. Osborne, R.J. Paxton, and M.J.F. Brown. 2014. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506: 364–366. doi: 10.1038/nature12977.CrossRefGoogle Scholar
  17. Gallai, N., J.-M. Salles, J. Settele, and B.E. Vaissière. 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68: 810–821. doi: 10.1016/j.ecolecon.2008.06.014.CrossRefGoogle Scholar
  18. Garibaldi, L., I. Steffan-Dewenter, R. Winfree, M.A. Aizen, R. Bommarco, S.A. Cunningham, C. Kremen, L.G. Carvalheiro, et al. 2013. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339: 1608–1611. doi: 10.1126/science.1230200.CrossRefGoogle Scholar
  19. Genersch, E., C. Yue, I. Fries, and J.R. de Miranda. 2006. Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. Journal of Invertebrate Pathology 91: 61–63. doi: 10.1016/j.jip.2005.10.002.CrossRefGoogle Scholar
  20. Gordon, J., and L. Davis. 2003. Valuing honeybee pollination. Rural Industries Research and Development Corporation. 03/077.Google Scholar
  21. Goulson, D., J.C. Stout, and A.R. Kells. 2002. Do exotic bumblebees and honeybees compete with native flower-visiting insects in Tasmania? Journal of Insect Conservation 6: 179–189. doi: 10.1023/A:1023239221447.CrossRefGoogle Scholar
  22. Harbo, J.R., and J.W. Harris. 2001. Resistance to Varroa destructor (Mesostigmata: Varroidae) when mite-resistant queen honey bees (Hymenoptera: Apidae) were free-mated with unselected drones. Journal of Economic Entomology 94: 1319–1323. doi: 10.1603/0022-0493-94.6.1319.CrossRefGoogle Scholar
  23. Hingston, A., and P. McQuillan. 1999. Displacement of Tasmanian native megachilid bees by the recently introduced bumblebee Bombus terrestris (Linnaeus, 1758) (Hymenoptera: Apidae). Australian Journal of Zoology 47: 59–65.CrossRefGoogle Scholar
  24. Hingston, A.B., J. Marsden-Smedley, D.A. Driscoll, S. Corbett, J. Fenton, R. Anderson, C. Plowman, F. Mowling, et al. 2002. Extent of invasion of Tasmanian native vegetation by the exotic bumblebee Bombus terrestris (Apoidea: Apidae). Austral Ecology 27: 162–172. doi: 10.1046/j.1442-9993.2002.01179.x.CrossRefGoogle Scholar
  25. Howlett, B., and B. Donovan. 2010. A review of New Zealand’s deliberately introduced bee fauna: Current status and potential impacts. New Zealand Entomologist 33: 92–101.CrossRefGoogle Scholar
  26. Huryn, V.M.B. 1995. Use of native New Zealand plants by honey bees (Apis mellifera L.): A review. New Zealand Journal of Botany 33: 497–512.CrossRefGoogle Scholar
  27. Iwasaki, J. Unpublished data, Department of Botany, University of Otago, Dunedin, New Zealand.Google Scholar
  28. Jaffé, R., V. Dietemann, M.H. Allsopp, C. Costa, R.M. Crewe, R. Dall’olio, P. de la Rúa, M.A.A. El-niweiri, et al. 2010. Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses. Conservation Biology 24: 583–593. doi: 10.1111/j.1523-1739.2009.01331.x.CrossRefGoogle Scholar
  29. Johnson, R.M., M.D. Ellis, C.A. Mullin, and M. Frazier. 2010. Pesticides and honey bee toxicity—USA. Apidologie 41: 312–331.CrossRefGoogle Scholar
  30. Kingston, A.B., and P.B. McQuillan. 1998. Does the recently introduced bumblebee Bombus terrestris (Apidae) threaten Australian ecosystems? Australian Journal of Ecology 23: 539–549.CrossRefGoogle Scholar
  31. Klein, A.-M., B.E. Vaissière, J.H. Cane, I. Steffan-Dewenter, S.A. Cunningham, C. Kremen, and T. Tscharntke. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society: Biological Sciences 274: 303–313. doi: 10.1098/rspb.2006.3721.CrossRefGoogle Scholar
  32. Kremen, C., N.M. Williams, and R.W. Thorp. 2002. Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences of the United States of America 99: 16812–16816. doi: 10.1073/pnas.262413599.CrossRefGoogle Scholar
  33. Ledgard, S.F., M.S. Sprosen, J.W. Penno, and G.S. Rajendram. 2001. Nitrogen fixation by white clover in pastures grazed by dairy cows: Temporal variation and effects of nitrogen fertilization. Plant and Soil 299: 177–187.CrossRefGoogle Scholar
  34. Lockwood, J.L., M.F. Hoopes, and M.P. Marchetti. 2013. Invasion ecology. London: Wiley.Google Scholar
  35. Mark, G., and V. Cliff. 2001. Control of Varroa (a guide for New Zealand Beekeepers). Willington: New Zealand Ministry of Agriculture and Forestry.Google Scholar
  36. Martin, S.J., and L.M. Medina. 2004. Africanized honeybees have unique tolerance to Varroa mites. Trends in Parasitology 20: 113–114. doi: 10.1016/j.pt.2003.12.005.CrossRefGoogle Scholar
  37. Martin, S.J., A.C. Highfield, L. Brettell, E.M. Villalobos, G.E. Budge, M. Powell, S. Nikaido, and D.C. Schroeder. 2012. Global honey bee viral landscape altered by a parasitic mite. Science 336: 1304–1306. doi: 10.1126/science.1220941.CrossRefGoogle Scholar
  38. McMenamin, A.J., and E. Genersch. 2015. Honey bee (Apis mellifera) colony losses and associated viruses. Current Opinion in Insect Science 2: 1–9. doi: 10.1016/j.cois.2015.01.015.CrossRefGoogle Scholar
  39. Ministry for Primary Industries. 2013. Varroa mite. Retrieved 26 March, 2015, from http://www.biosecurity.govt.nz/pests/varroa.
  40. Ministry for Primary Industries. 2014. 2014 Apiculture Monitoring Report. doi: 10.1111/j.1747-0080.2007.00199.x.
  41. Ministry of Agriculture and Forestry. 2000. Varroa in New Zealand: Economic impact assessment. Auckland: Ministry of Agriculture and Forestry.Google Scholar
  42. Ministry of Agriculture and Forestry. 2002a. Management of biosecurity risks: Case studies. Willington: Ministry of Agriculture and Forestry.Google Scholar
  43. Ministry of Agriculture and Forestry. 2002b. Review of Varroa economic impact assessment: Recommendations on revision, vol. 1. Canberra: Ministry of Agriculture and Forestry.Google Scholar
  44. Ministry of Agriculture and Forestry. 2003a. Major changes to Varroa movement controls. Retrieved 26 March, 2015, from https://web.archive.org/web/20130208175132/http://mpi.govt.nz/news-resources/news/major-changes-to-varroa-movement-controls.aspx.
  45. Ministry of Agriculture and Forestry. 2003b. Varroa pest management strategy outlined. Retrieved 26 March, 2015, from https://web.archive.org/web/20130208174554/http://mpi.govt.nz/news-resources/news/varroa-pest-management-strategy-outlined.aspx.
  46. Ministry of Agriculture and Forestry. 2004a. No further finds of Varroa in South Island. Retrieved 26 March, 2015, from https://web.archive.org/web/20130208185754/http://mpi.govt.nz/news-resources/news/no-further-finds-of-varroa-in-south-island.aspx.
  47. Ministry of Agriculture and Forestry. 2004b. South Island Varroa update. Retrieved 26 March, 2015, from https://web.archive.org/web/20130208185805/http:/mpi.govt.nz/news-resources/news/south-island-varroa-update.aspx.
  48. Ministry of Agriculture and Forestry. 2004c. Varroa investigation continues. Retrieved 26 March, 2015, from https://web.archive.org/web/20130206220404/http://mpi.govt.nz/news-resources/news/varroa-investigation-continues.
  49. Ministry of Agriculture and Forestry. 2006a. Nelson Varroa bee mite incursion—Update 3. Retrieved 26 March, 2015, from https://web.archive.org/web/20130216161132/http://mpi.govt.nz/news-resources/news/nelson-varroa-bee-mite-incursion-update-3.aspx.
  50. Ministry of Agriculture and Forestry. 2006b. Varroa update 15. Retrieved 26 March, 2015, from https://web.archive.org/web/20130216170505/http://mpi.govt.nz/news-resources/news/varroa-update-15.aspx.
  51. Ministry of Agriculture and Forestry. 2007. Varroa update 18. Retrieved 26 March, 2015, from https://web.archive.org/web/20130216171009/http://mpi.govt.nz/news-resources/news/varroa-update-18.aspx.
  52. Ministry of Agriculture and Forestry. 2008a. MAF biosecurity to revoke varroa movement controls. Retrieved 26 March, 2015, from https://web.archive.org/web/20130216180955/http://mpi.govt.nz/news-resources/news/maf-biosecurity-to-revoke-varroa-movement-controls.aspx.
  53. Ministry of Agriculture and Forestry. 2008b. New South Island controlled area for Varroa bee mite. Retrieved 26 March, 2015, from https://web.archive.org/web/20130216172053/http://mpi.govt.nz/news-resources/news/new-south-island-controlled-area-for-varroa-bee-mi.aspx.
  54. Mondet, F., J.R. de Miranda, A. Kretzschmar, Y. Le Conte, and A.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 10: 1–15. doi: 10.1371/journal.ppat.1004323.CrossRefGoogle Scholar
  55. Oldroyd, B. 1999. Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees. Trends in Ecology & Evolution 14: 312–315.CrossRefGoogle Scholar
  56. Oldroyd, B.P., E. Thexton, S. Lawler, and R. Crozier. 1997. Population demography of Australian feral bees (Apis mellifera). Oecologia 111: 381–387.CrossRefGoogle Scholar
  57. Paini, D., and J. Roberts. 2005. Commercial honey bees reduce the fecundity of an Australian native bee. Biological Conservation 123: 103–112. doi: 10.1016/j.biocon.2004.11.001.CrossRefGoogle Scholar
  58. Paini, D.R. 2004. Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: A review. Austral Ecology 29: 399–407. doi: 10.1111/j.1442-9993.2004.01376.x.CrossRefGoogle Scholar
  59. Parliamentary Commissioner for the Environment. 2013. Water quality in New Zealand: Land use and nutrient pollution. Retrieved 26 March, 2015, from http://www.pce.parliament.nz/assets/Uploads/PCE-Water-quality-land-use-web-amended.pdf.
  60. Paton, D.C. 1993. Honeybees in the Australian environment. BioScience 43: 95–103.CrossRefGoogle Scholar
  61. Popic, T.J., G.M. Wardle, and Y.C. Davila. 2013. Flower-visitor networks only partially predict the function of pollen transport by bees. Austral Ecology 38: 76–86. doi: 10.1111/j.1442-9993.2012.02377.x.CrossRefGoogle Scholar
  62. Potts, S.G., J.C. Biesmeijer, C. Kremen, P. Neumann, O. Schweiger, and W.E. Kunin. 2010. Global pollinator declines: Trends, impacts and drivers. Trends in Ecology & Evolution 25: 345–353. doi: 10.1016/j.tree.2010.01.007.CrossRefGoogle Scholar
  63. Rader, R., B.G. Howlett, S.A. Cunningham, D.A. Westcott, L.E. Newstrom-Lloyd, M.K. Walker, D.A.J.J. Teulon, and W. Edwards. 2009. Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop. Journal of Applied Ecology 46: 1080–1087. doi: 10.1111/j.1365-2664.2009.01700.x.CrossRefGoogle Scholar
  64. Rader, R., B.G. Howlett, S.A. Cunningham, D.A. Westcott, and W. Edwards. 2012. Spatial and temporal variation in pollinator effectiveness: Do unmanaged insects provide consistent pollination services to mass flowering crops? Journal of Applied Ecology 49: 126–134. doi: 10.1111/j.1365-2664.2011.02066.x.CrossRefGoogle Scholar
  65. Ravoet, J., L. De Smet, I. Meeus, G. Smagghe, T. Wenseleers, and D.C. de Graaf. 2014. Widespread occurrence of honey bee pathogens in solitary bees. Journal of Invertebrate Pathology 122: 55–58. doi: 10.1016/j.jip.2014.08.007.CrossRefGoogle Scholar
  66. Ricketts, T. 2004. Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conservation Biology 18: 1262–1271.CrossRefGoogle Scholar
  67. Rinderer, T.E., B.P. Oldroyd, A.M. Frake, L.I. de Guzman, and L. Bourgeois. 2013. Responses to Varroa destructor and Nosema ceranae by several commercial strains of Australian and North American honeybees (Hymenoptera: Apidae). Australian Journal of Entomology 52: 156–163. doi: 10.1111/aen.12003.CrossRefGoogle Scholar
  68. Ritter, Wolfgang. 1981. Varroa disease of the honeybee Apis mellifera. Bee World 62: 141–153.CrossRefGoogle Scholar
  69. Roberts, J. 2015. Email communication. Canberra: CSIRO ecosystem Sciences/Biosecurity Flagship.Google Scholar
  70. Rosenkranz, P., P. Aumeier, and B. Ziegelmann. 2010. Biology and control of Varroa destructor. Journal of Invertebrate Pathology 103: S96–S119. doi: 10.1016/j.jip.2009.07.016.CrossRefGoogle Scholar
  71. Stout, J.C., A.R. Kells, and D. Goulson. 2002. Pollination of the invasive exotic shrub Lupinus arboreus (Fabaceae) by introduced bees in Tasmania. Biological Conservation 106: 425–434. doi: 10.1016/S0006-3207(02)00046-0.CrossRefGoogle Scholar
  72. Waters, J.M., and D. Craw. 2006. Goodbye Gondwana? New Zealand biogeography, geology, and the problem of circularity. Systematic Biology 55: 351–356.CrossRefGoogle Scholar
  73. Williams, G.R., D.R. Tarpy, D. VanEngelsdorp, M.P. Chauzat, D.L. Cox-Foster, K.S. Delaplane, P. Neumann, J.S. Pettis, et al. 2010. Colony collapse disorder in context. BioEssays 32: 845–846. doi: 10.1002/bies.201000075.CrossRefGoogle Scholar

Copyright information

© Royal Swedish Academy of Sciences 2015

Authors and Affiliations

  • Jay M. Iwasaki
    • 1
    • 2
  • Barbara I. P. Barratt
    • 1
    • 3
  • Janice M. Lord
    • 1
  • Alison R. Mercer
    • 2
  • Katharine J. M. Dickinson
    • 1
  1. 1.Department of BotanyUniversity of OtagoDunedinNew Zealand
  2. 2.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  3. 3.Invermay Agricultural Centre, Puddle AlleyMosgielNew Zealand

Personalised recommendations