Mycological Progress

, 15:55 | Cite as

Scolytus multistriatus associated with Dutch elm disease on the island of Gotland: phenology and communities of vectored fungi

  • Audrius Menkis
  • Inga-Lena Östbrant
  • Kateryna Davydenko
  • Remigijus Bakys
  • Maksims Balalaikins
  • Rimvydas Vasaitis
Original Article


Scolytus multistriatus Marsham, the smaller European elm bark beetle, is a vector for Dutch elm disease (DED) that in the year 2005 invaded the island of Gotland (Sweden). The island possesses the largest population of elm (mainly Ulmus minor Mill.) in northern Europe. The aim of this study was to monitor flying periods of S. multistriatus during three consecutive years and by using high-throughput sequencing to assess communities of vectored fungi. Sampling of the beetles was carried out at two different sites in Gotland in 2012, 2013, and 2014. In total, 50 pheromone traps were placed at each site and checked weekly during June-August each year. From all sites and years, 177 beetles were trapped. Among these, 6.2 % were trapped in June, 76.8 % in July, and 16.9 % in August (difference significant at p<0.007). Sequencing of ITS rDNA from the beetles revealed the presence of 1589 fungal taxa, among which virulent DED pathogen Ophiostoma novo-ulmi Brasier was the second most common species (9.0 % of all fungal sequences). O. ulmi Buisman, the less virulent DED pathogen, was also detected but only in a single beetle, which was sampled in 2012 (0.04 % of sequences). There were 13.0 % of the beetles infested with O. novo-ulmi in 2012, 4.0 % in 2013, and 27.7 % in 2014. O. novo-ulmi comprised 0.8 % of fungal sequences in 2012, 0.002 % in 2013, and 8.2 % in 2014. The study showed that the proportion of S. multistriatus vectoring O. novo-ulmi has increased in recent years.


Ophiostoma Invasive pathogens Bark beetles Disease management Fungal community Ulmus 



We thank Diem Nguyen at the Dept. of Forest Mycology and Plant Pathology, SLU, for language revision and Karin Wågström at the Swedish Forest Agency for help with the field work. The financial support is gratefully acknowledged from Foundation Oscar and Lili Lamms Minne, Carl Tryggers Foundation, the Swedish Research Council Formas, and the EU Life+ Nature Elmias (LIFE12 NAT/SE/001139) project.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11557_2016_1199_MOESM1_ESM.pdf (472 kb)
Supplementary Table 1 (PDF 472 kb)


  1. Bartels JM, Lanier GN (1974) Emergence and mating in Scolytus multistriatus (Coleoptera, Scolytidae). Ann Entomol Soc Am 67:365–370CrossRefGoogle Scholar
  2. Bellows TS, Meisenbacher C, Reardon RC (1998) European elm bark beetle biological control. Paper presented at the Biological control of arthropod forest pests of the western United States: a review and recommendations. USDA Forest Service, FHTET–96–21, The University of Georgia, and Southern Forest Insect Work Conference. Available from Accessed 15 January 2016
  3. Bernier L, Aoun M, Bouvet GF, Comeau A, Dufour J, Naruzawa ES, Nigg M, Plourde KV (2014) Genomics of the Dutch elm disease pathosystem: are we there yet? iForest 8:149–157. doi: 10.3832/ifor1211-008 CrossRefGoogle Scholar
  4. Brasier CM, Mehrotra MD (1995) Ophiostoma himal-ulmi sp. nov., a new species of Dutch elm disease fungus endemic to the Himalayas. Mycol Res 99:205–215CrossRefGoogle Scholar
  5. Brasier CM, Buck K, Paoletti M, Crawford L, Kirk S (2004) Molecular analysis of evolutionary changes in populations of Ophiostma novo-ulmi. For Res Syst 13:93–103Google Scholar
  6. Brockerhoff EG, Knížek M, Bain J (2003) Checklist of indigenous and adventive bark and ambrosia beetles (Curculionidae: Scolytinae and Platypodinae) of New Zealand and interceptions of exotic species (1952–2000). N Z Entomol 26:29–44. doi: 10.1080/00779962.2003.9722106 CrossRefGoogle Scholar
  7. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc London Ser Biol Sci 345:101–118CrossRefGoogle Scholar
  8. Davydenko K, Vasaitis R, Meshkova V, Menkis A (2014) Fungi associated with the red-haired bark beetle, Hylurgus ligniperda (Coleoptera: Curculionidae) in the forest-steppe zone in eastern Ukraine. Eur J Entomol 111:561–565. doi: 10.14411/eje.2014.070 Google Scholar
  9. Domsch KH, Gams W, Anderson TH (2007) Compendium of soil fungi. IHW-Verlag, EchingGoogle Scholar
  10. Edde PA, Toews MD, Phillips TW (2011) Effects of various semiochemicals on the responses of Rhyzopertha dominica to pheromone traps in the field. Ann Entomol Soc Am 104:1297–1302. doi: 10.1603/an11090 CrossRefGoogle Scholar
  11. Giordano L, Garbelotto M, Nicolotti G, Gonthier P (2012) Characterization of fungal communities associated with the bark beetle Ips typographus varies depending on detection method, location, and beetle population levels. Mycol Prog 12:127–140. doi: 10.1007/s11557-012-0822-1 CrossRefGoogle Scholar
  12. Houle C, Hartmann GC, Wasti SS (1987) Infectivity of 8 species of entomogenous fungi to the larvae of the elm bark beetle, Scolytus multistriatus (Marsham). J NY Entomol Soc 95:14–18Google Scholar
  13. Ihrmark K, Bodeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandstrom-Durling M, Clemmensen KE, Lindahl BD (2012) New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 82:666–677. doi: 10.1111/j.1574-6941.2012.01437.x CrossRefPubMedGoogle Scholar
  14. Johnson PL, Hayes JL, Rinehart J, Sheppard WS, Smith SE (2008) Characterization of two non-native invasive bark beetles, Scolytus schevyrewi and Scolytus multistriatus (Coleoptera: Curculionidae: Scolytinae). Can Entomol 140:527–538CrossRefGoogle Scholar
  15. Kirisits T (2013) Dutch Elm Disease and Other Ophiostoma Diseases. In:Gonthier P, Nicolotti G (eds) Infectious Forest Diseases. CABI, pp 256–282Google Scholar
  16. Kolarik M, Jankowiak R (2013) Vector affinity and diversity of Geosmithia fungi living on subcortical insects inhabiting Pinaceae species in central and northeastern Europe. Microb Ecol 66:682–700. doi: 10.1007/s00248-013-0228-x CrossRefPubMedGoogle Scholar
  17. Kolarik M, Kubatova A, Hulcr J, Pazoutova S (2008) Geosmithia fungi are highly diverse and consistent bark beetle associates: Evidence from their community structure in temperate europe. Microb Ecol 55:65–80. doi: 10.1007/s00248-007-9251-0 CrossRefPubMedGoogle Scholar
  18. Lee JC, Aguayo I, Aslin R, Durham G, Hamud SM, Moltzan BD, Munson AS, Negron JF, Peterson T, Ragenovich IR, Witcosky JJ, Seybold SJ (2009) Co-occurrence of the invasive banded and European elm bark beetles (Coleoptera: Scolytidae) in North America. Ann Entomol Soc Am 102:426–436CrossRefGoogle Scholar
  19. Lim YW, Kim JJ, Lu M, Breuil C (2005) Determining fungal diversity on Dendroctonus ponderosae and Ips pini affecting lodgepole pine using cultural and molecular methods. Fungal Divers 19:79–94Google Scholar
  20. Mead R, Curnow RN (1983) Statistical methods in agriculture and experimental biology. Chapman & Hall, LondonCrossRefGoogle Scholar
  21. Menkis A, Urbina H, James TY, Rosling A (2014) Archaeorhizomyces borealis sp. nov. and a sequence-based classification of related soil fungal species. Fungal Biol 118:943–955. doi: 10.1016/j.funbio.2014.08.005 CrossRefPubMedGoogle Scholar
  22. Menkis A, Östbrant I-L, Wågström K, Vasaitis R (2016) Dutch elm disease on the island of Gotland: monitoring disease vector and combat measures. Scand J For Res 31:237–241. doi: 10.1080/02827581.2015.1076888 CrossRefGoogle Scholar
  23. Östbrant IL, Wågström K, Persson M, Smedberg AL (2009) Holländsk almsjuka. Ophiostoma novo-ulmi i Gotlands län år 2009 Dutch elm disease. Ophiostoma novo-ulmi in county of Gotland year 2009. Länsstyrelsen Gotlands Län, Dnr:640-7109-09 (In Swedish)Google Scholar
  24. Paine TD, Birch MC, Miller JC (1984) Use of pheromone traps to suppress populations of Scolytus multistriatus (Marsham) (Coleoptera, Solytidae) in 3 isolated communities of elms. Agric Ecosyst Environ 11:309–318. doi: 10.1016/0167-8809(84)90004-5 CrossRefGoogle Scholar
  25. Parbery DG, Rumba KA (1991) Michenera artocreas in elm wood infested with Scolytus multistriatus in Australia. Mycol Res 95:761–762. doi: 10.1016/S0953-7562(09)80829-0 CrossRefGoogle Scholar
  26. Persson Y, Vasaitis R, Langstrom B, Ohrn P, Ihrmark K, Stenlid J (2009) Fungi vectored by the bark beetle Ips typographus following hibernation under the bark of standing trees and in the forest litter. Microb Ecol 58:651–659. doi: 10.1007/s00248-009-9520-1 CrossRefPubMedGoogle Scholar
  27. Phillips DH, Burdekin DA (1982) Diseases of forest and ornamental trees. The Macmillan Press, LondonCrossRefGoogle Scholar
  28. Ploetz RC, Hulcr J, Wingfield MJ, de Beer ZW (2013) Destructive tree diseases associated with ambrosia and bark beetles: black swan events in tree pathology? Plant Dis 97:856–872. doi: 10.1094/pdis-01-13-0056-fe CrossRefGoogle Scholar
  29. Porazinska DL, Sung W, Giblin-Davis RM, Thomas WK (2010) Reproducibility of read numbers in high-throughput sequencing analysis of nematode community composition and structure. Mol Ecol Resour 10:666–676. doi: 10.1111/j.1755-0998.2009.02819.x CrossRefPubMedGoogle Scholar
  30. Rosling A, Cox F, Cruz-Martinez K, Ihrmark K, Grelet GA, Lindahl BD, Menkis A, James TY (2011) Archaeorhizomycetes: unearthing an ancient class of ubiquitous soil fungi. Science 333:876–879. doi: 10.1126/science.1206958 CrossRefPubMedGoogle Scholar
  31. Santini A, Faccoli M (2015) Dutch elm disease and elm bark beetles: a century of association (Dutch elm disease and elm bark beetles: a century of association). iForest 8:126–134. doi: 10.3832/ifor1231-008 CrossRefGoogle Scholar
  32. Schlyter F, Anderbrant O, Lindquist G, Jansson A (1987) Dutch elm disease (Ceratocystis ulmi) and elm bark beetles in Malmö town 1985 - distribution, phenology and practical measures in an integrated control program. Vaxtskyddsnotiser 51:2–10Google Scholar
  33. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W.H. Freeman and Co, New YorkGoogle Scholar
  34. Vega FE, Blackwell M (2005) Insect-fungal associations: ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  35. Wang Y-P, Guo R, Deng J-Y, Zhang Z (2014) Field efficacy of combinations of attractants for bark beetles and longicorn beetles in trapping wood-boring beetles. Acta Entomol Sin 56:452–456Google Scholar
  36. Webber JF (1990) Relative effectiveness of Scolytus scolytus, S. multistriatus and S. kirschi as vectors of Dutch elm disease. Eur J For Pathol 20:184–192. doi: 10.1111/j.1439-0329.1990.tb01129.x CrossRefGoogle Scholar
  37. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: A guide to methods and applications. Academic Press, Inc, San Diego, pp 315–322Google Scholar
  38. Wood SL (1982) The bark and ambrosia beetles of North and Central America (Coleoptera: Scolytidae), a taxonomic monograph. Great Basin Nat Mem 6:1–359Google Scholar

Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Audrius Menkis
    • 1
  • Inga-Lena Östbrant
    • 2
  • Kateryna Davydenko
    • 3
  • Remigijus Bakys
    • 4
  • Maksims Balalaikins
    • 5
  • Rimvydas Vasaitis
    • 1
  1. 1.Department of Forest Mycology and Plant Pathology, Uppsala BioCenterSwedish University of Agricultural SciencesUppsalaSweden
  2. 2.Swedish Forest Agency Gotland DistrictVisbySweden
  3. 3.Ukrainian Research Institute of Forestry and Forest MeliorationKharkivUkraine
  4. 4.Institute of Forest Biology and SilvicultureAleksandras Stulginskis UniversityAkademija Kaunas DistrictLithuania
  5. 5.Institute of Life Sciences and TechnologyDaugavpils UniversityDaugavpilsLatvia

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