Parasitology Research

, Volume 112, Issue 2, pp 751–759 | Cite as

The microsporidian parasites Nosema ceranae and Nosema apis are widespread in honeybee (Apis mellifera) colonies across Scotland

  • Karen A Bollan
  • J. Daniel Hothersall
  • Christopher Moffat
  • John Durkacz
  • Nastja Saranzewa
  • Geraldine A. Wright
  • Nigel E. Raine
  • Fiona Highet
  • Christopher N. ConnollyEmail author
Original Paper


Nosema ceranae is spreading into areas where Nosema apis already exists. N. ceranae has been reported to cause an asymptomatic infection that may lead, ultimately, to colony collapse. It is thought that there may be a temperature barrier to its infiltration into countries in colder climates. In this study, 71 colonies from Scottish Beekeeper’s Association members have been screened for the presence of N. apis and N. ceranae across Scotland. We find that only 11 of the 71 colonies tested positive for spores by microscopy. However, 70.4 % of colonies screened by PCR revealed the presence of both N. ceranae and N. apis, with only 4.2 or 7 % having either strain alone and 18.3 % being Nosema free. A range of geographically separated colonies testing positive for N. ceranae were sequenced to confirm their identity. All nine sequences confirmed the presence of N. ceranae and indicated the presence of a single new variant. Furthermore, two of the spore-containing colonies had only N. ceranae present, and these exhibited the presence of smaller spores that could be distinguished from N. apis by the analysis of average spore size. Differential quantification of the PCR product revealed N. ceranae to be the dominant species in all seven samples tested. In conclusion, N. ceranae is widespread in Scotland where it exists in combination with the endemic N. apis. A single variant, identical to that found in France (DQ374655) except for the addition of a single nucleotide polymorphism, is present in Scotland.


Varroa Destructor Insect Pollinator Fumagillin Honey Production Small Spore 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank the Scottish Beekeeper’s Association for their support in obtaining all the samples from their members across Scotland and the individual beekeepers participating, including Phil McAnespie, John Coyle, Alan Riach, Jim Ferguson, Helga Irvine, Ann Chilcott, Eric McArthur, and Mike Thornley. We also thank Bethany and Elaine Burch for technical assistance with the preparation of the samples. This study was supported by The Insect Pollinator Initiative (funded under the auspices of the Living with Environmental Change programme, by the Biotechnology and Biological Sciences Research Council, the Wellcome Trust, the Scottish Government, the Department for Environment, Food and Rural Affairs, and the Natural Environment Research Council (Ref. nos. BB/I00031/1 to CNC, BB/I000143/1 to GR and BB/I000178/1 to NR).

Supplementary material

436_2012_3195_MOESM1_ESM.doc (340 kb)
Supplementary Figure 1 Size distribution of Nosema spores identified in Scotland using larger dataset. a Samples were distributed into two groups [group A (221 spores); samples 31, 34 and 66] and [group B (171 spores); samples15, 17, 18, and 42] based on size differences determined by ANOVA (Kruskal–Wallis; Dunnett’s post hoc test) and analyzed for length, width and square area. Data were analyzed using a Mann–Whitney test (*P < 0.001). b The scatter of the length, width and square area of the spores in each sample were plotted to illustrate their size distribution. Red lines represent the average of each dataset. (DOC 339 kb). (DOC 339 kb)


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Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Karen A Bollan
    • 1
  • J. Daniel Hothersall
    • 1
  • Christopher Moffat
    • 1
  • John Durkacz
    • 1
  • Nastja Saranzewa
    • 1
  • Geraldine A. Wright
    • 2
  • Nigel E. Raine
    • 3
  • Fiona Highet
    • 4
  • Christopher N. Connolly
    • 1
    Email author
  1. 1.Division of Neuroscience, Medical Research Institute, Ninewells Medical SchoolUniversity of DundeeDundeeUK
  2. 2.Institute of Neuroscience, School of Biology, Ridley BuildingNewcastle UniversityNewcastle upon TyneUK
  3. 3.School of Biological Sciences, Royal HollowayUniversity of LondonEgham, SurreyUK
  4. 4.Science and Advice for Scottish AgricultureEdinburghUK

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