Antonie van Leeuwenhoek

, Volume 109, Issue 7, pp 987–1018 | Cite as

The Ophiostoma clavatum species complex: a newly defined group in the Ophiostomatales including three novel taxa

  • Riikka LinnakoskiEmail author
  • Robert Jankowiak
  • Caterina Villari
  • Thomas Kirisits
  • Halvor Solheim
  • Z. Wilhelm de Beer
  • Michael J. Wingfield
Original Paper


Two species of blue-stain fungi with similar morphologies, Ophiostoma brunneo-ciliatum and Ophiostoma clavatum, are associates of bark beetles infesting Pinus spp. in Europe. This has raised questions whether they represent distinct taxa. Absence of herbarium specimens and contaminated or mistakenly identified cultures of O. brunneo-ciliatum and O. clavatum have accentuated the uncertainty regarding their correct identification. The aim of this study was to reconsider the identity of European isolates reported as O. brunneo-ciliatum and O. clavatum by applying DNA-based identification methods, and to provide appropriate type specimens for them. Phylogenetic analyses of the ITS, βT, TEF-1α and CAL gene sequences revealed that the investigated isolates represent a complex of seven cryptic species. The study confirmed that ITS data is insufficient to delineate species in some Ophiostoma species clusters. Lectotypes and epitypes were designated for O. clavatum and O. brunneo-ciliatum, and three new species, Ophiostoma brunneolum, Ophiostoma macroclavatum and Ophiostoma pseudocatenulatum, are described in the newly defined O. clavatum-complex. The other two species included in the complex are Ophiostoma ainoae and Ophiostoma tapionis. The results suggest co-evolution of these fungi in association with specific bark beetles. The results also confirm the identity of the fungus associated with the pine bark beetle Ips acuminatus as O. clavatum, while O. brunneo-ciliatum appears to be mainly associated with another pine bark beetle, Ips sexdentatus.


Bark beetle-associated fungi Ophiostomatoid fungi Ophiostoma brunneolum Ophiostoma macroclavatum Ophiostoma pseudocatenulatum 



We thank Stefan Ekman and Anders Nording at the Museum of Evolution, University of Uppsala, for providing facilities and their help to study the UPS herbarium specimens. The Nikon microscope and SEM images were taken at the School of Forest Sciences and at the Department of Physics and Mathematics, University of Eastern Finland, respectively. We acknowledge Ari Pappinen, Pertti Pääkkönen and Tommi Itkonen for providing facilities and their help to conduct the above mentioned microscopy. An isolate previously identified as O. brunneo-ciliatum was obtained as a kind concession of Francois Lieutier and Annie Yart, Institut National de la Recherche Agronomique (INRA), Orleans, France. Gernot Hoch at the Federal Research and Training Centre for Forest, Natural Hazards and Landscape, Vienna, kindly provided pine material infested by I. acuminatus in Southern Austria, from which O. clavatum was isolated. Specifically acknowledged is also Johanna Ahtiainen, who collected many isolates investigated in this study. We are most grateful for our numerous colleagues, laboratory technicians and assistants for their invaluable help with isolating and maintaining the fungal cultures used in this study. We also thank the three anonymous reviewers whose comments helped improving this article. The study was supported financially by the University of Helsinki and the Emil Aaltonen Foundation, Finland; the University of Pretoria, the members of the Tree Protection Co-operative Programme (TPCP) and the THRIP initiative of the Department of Trade and Industry, South Africa; the Ministry of Science and Higher Education of the Republic of Poland; Ministero dell’Istruzione, dell’Università e della Ricerca (PRIN 200774ENMR ‘Climatic change and Italian pine pests: a model study’), Italy; the European Union’s Seventh Framework Programme FP7/2007–2013 (KBBE 2009-3) under grant agreement 245268 ISEFOR; and the Norwegian Biodiversity Information Centre (pnr. 70184233).


  1. Altenkirch W, Majunke C, Ohnesorge B (2002) Waldschutz auf ökologischer Grundlage. Verlag Eugen Ulmer, StuttgartGoogle Scholar
  2. Aoshima K (1965) Studies on wood-staining fungi of Japan. Dissertation, University of Tokyo (in Japanese)Google Scholar
  3. Ariyawansa HA, Hawksworth DL, Hyde KD, Jones EBG, Maharachchikumbura SSN, Manamgoda DS, Thambugala KM, Udayanga D, Camporesi E, Daranagama A, Jayawardena R, Liu J-K, McKenzie EHC, Phookamsak R, Senanayake IC, Shivas RG, Tian Q, Xu JC (2014) Epitypification and neotypification: guidelines with appropriate and inappropriate examples. Fungal Divers 69:57–91CrossRefGoogle Scholar
  4. ArtDatabanken (2015) Rödlista 2010. ArtDatabanken, SLU, Uppsala, Sweden. Accessed April 2015
  5. Bueno A, Diez JJ, Fernández MM (2010) Ophiostomatoid fungi transported by Ips sexdentatus (Coleoptera; Scolytidae) in Pinus pinaster in NW Spain. Silva Fenn 44:387–397CrossRefGoogle Scholar
  6. Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556CrossRefGoogle Scholar
  7. Colombari F, Battisti A, Schroeder LM, Faccoli M (2012) Life-history traits promoting outbreaks of the pine bark beetle Ips acuminatus (Coleoptera: Curculionidae, Scolytinae) in the south-eastern Alps. Eur J For Res 3:553–561. doi: 10.1007/s10342-011-0528-y CrossRefGoogle Scholar
  8. Colombari F, Schroeder M, Battisti A, Faccoli M (2013) Spatio-temporal dynamics of Ips acuminatus outbreak and implications for management. Agric For Entomol 15:34–42. doi: 10.1111/j.1461-9563.2012.00589.x CrossRefGoogle Scholar
  9. De Beer ZW, Wingfield MJ (2013) Emerging lineages in the Ophiostomatales: In: Seifert KA, De Beer ZW, Wingfield MJ (eds) Ophiostomatoid fungi: expanding frontiers. CBS Biodivers Ser 12:21–46Google Scholar
  10. De Beer ZW, Seifert KA, Wingfield MJ (2013) A nomenclator for ophiostomatoid genera and species in the Ophiostomatales and Microascales. In: Seifert KA, De Beer ZW, Wingfield MJ (eds) Ophiostomatoid fungi: expanding frontiers. CBS Biodivers Ser 12:261–268Google Scholar
  11. Dobbertin M, Wermelinger B, Bigler C, Bürgi M, Carron M, Foster B, Gimmi U, Rigling M (2007) Linking increasing drought stress to Scots pine mortality and bark beetle infestations. Sci World J 7:231–239. doi: 10.1100/tsw.2007.58 CrossRefGoogle Scholar
  12. Duong TA, De Beer ZW, Wingfield BD, Wingfield MJ (2012) Phylogeny and taxonomy of species in the Grosmannia serpens complex. Mycologia 104:715–732. doi: 10.385/11-109 CrossRefPubMedGoogle Scholar
  13. Francke-Grosmann H (1952) Über die Ambrosiazucht der beiden Kiefernborkenkäfer Myelophilus minor Htg. und Ips acuminatus Gyll. Medd Statens Skogsforskningsinst 41:1–52Google Scholar
  14. Francke-Grosmann H (1963) Die Übertragung der Pilzflora bei dem Borkenkäfer Ips acuminatus Gyll.: Ein Beitrag zur Kenntnis der Ipiden-Symbiosen. Z Angew Entomol 52:355–361CrossRefGoogle Scholar
  15. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes—application to the identification of mycorrhiza and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  16. Gebhardt H, Weiss M, Oberwinkler F (2005) Dryadomyces amasae: a nutritional fungus associated with ambrosia beetles of the genus Amasa (Coleoptera: Curculionidae, Scolytinae). Mycol Res 109:687–696CrossRefPubMedGoogle Scholar
  17. Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous Ascomycetes. Appl Environ Microbiol 61:1323–1330PubMedPubMedCentralGoogle Scholar
  18. Grobbelaar J, de Beer ZW, Bloomer P, Wingfield MJ, Wingfield BD (2010) Ophiostoma tsotsi sp. nov., a wound- infesting fungus of hardwood trees in Africa. Mycopathologia 169:413–423. doi: 10.1007/s11046-009-9267-8 CrossRefPubMedGoogle Scholar
  19. Grubelnik RJ (1998) Untersuchungen über die Zusammensetzung der Mycoflora von Ips typographus L. auf ausgewählten Wald-Standorten unter besonderer Berücksichtigung der pathogenen Art Ceratocystis polonica. Master/Diploma Thesis, Universität für Bodenkultur Wien (BOKU)Google Scholar
  20. Guérard N, Dreyer E, Lieutier F (2000) Interactions between Scots pine, Ips acuminatus (Gyll.) and Ophiostoma brunneo-ciliatum (Math.): estimation of the critical thresholds of attack and inoculation densities and effects on hydraulic properties in the stem. Ann For Sci 57:681–690. doi: 10.1051/forest:2000149 CrossRefGoogle Scholar
  21. Harding S (1989) The influence of mutualistic blue-stain fungi on bark beetle population dynamics. Dissertation, Royal Veterinary and Agricultural University CopenhagenGoogle Scholar
  22. Hausner G, Reid J (2003) Notes on Ceratocystis brunnea and some other Ophiostoma species based on partial ribosomal DNA sequence analysis. Can J Bot 81:865–876. doi: 10.1139/b03-080 CrossRefGoogle Scholar
  23. Hunt J (1956) Taxonomy of the genus Ceratocystis. Lloydia 19:1–59Google Scholar
  24. Jacobs K, Bergdahl DR, Wingfield MJ, Halik S, Seifert KA, Bright DE, Wingfield BD (2004) Leptographium wingfieldii introduced into North America and found associated with exotic Tomicus piniperda and native bark beetles. Mycol Res 108:411–418. doi: 10.1017/S0953756204009748 CrossRefPubMedGoogle Scholar
  25. Jankowiak R (2004) Ophiostomatoid fungi associated with the spruce bark beetle (Ips typographus) new for Poland: occurrence and morphology. Phytopathol Pol 33:5–21Google Scholar
  26. Jankowiak R (2005) Fungi associated with Ips typographus on Picea abies in southern Poland and their succession into the phloem and sapwood of beetle-infested trees and logs. For Pathol 35:37–55Google Scholar
  27. Jankowiak R (2012) Ophiostomatoid fungi associated with Ips sexdentatus on Pinus sylvestris in Poland. Dendrobiology 68:43–54Google Scholar
  28. Jankowiak R, Kot M (2011) Ophiostomatoid fungi associated with bark beetles (Coleoptera: Scolytidae) colonizing branches of Pinus sylvestris in Southern Poland. Pol Bot J 56:287–293Google Scholar
  29. Jankowiak R, Rossa R, Místa K (2007) Survey of fungal species vectored by Ips cembrae to European larch trees in Raciborskie forests (Poland). Czech Mycol 59:227–239Google Scholar
  30. Jankowiak R, Kacprzyk M, Młynarczyk M (2009) Diversity of ophiostomatoid fungi associated with bark beetles (Coleoptera: Scolytidae) colonizing branches of Norway spruce (Picea abies) in southern Poland. Biologia 64:1170–1177. doi: 10.2478/s11756-009-0188-2 CrossRefGoogle Scholar
  31. Käärik A (1973) The succession of blueing fungi in insect galleries in roundwood during storage. Research Note No R 83. Royal College of Forestry, Department of Forest Products, Stockholm, Sweden, pp 1–20Google Scholar
  32. Käärik A (1975a) Insekter och blånad. Uppsatser/Sveriges Lantbruksuniversitet, Institutionen för Virkeslära, 0349-8913; 54 Skogs- och Virkesskydd, pp. 170–187Google Scholar
  33. Käärik A (1975b) Succession of microorganisms during wood decay. In: Biological transformation of wood by microorganisms. In: Liese W (ed) Proceedings of the sessions on wood products pathology at the 2nd international congress of plant pathology, 10–12 September 1973, Minneapolis, USA. Springer-Verlag, Berlin, pp 39–51Google Scholar
  34. Käärik A (1980) Fungi causing sap stain in wood. The Swedish University of Agricultural Sciences, Department of Forest Products. Report Nr R 114Google Scholar
  35. Kålås J, Viken Å, Henriksen S, Skjelseth S (eds) (2010) The 2010 Norwegian red list for species. Norwegian Biodiversity Information Centre, NorwayGoogle Scholar
  36. Katoh K, Standley D (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi: 10.1093/molbev/mst010 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kirisits T (2001) Studies on the association of ophiostomatoid fungi with bark beetles in Austria with special emphasis on Ips typographus and Ips cembrae and their associated fungi Ceratocystis polonica and Ceratocystis laricicola. Dissertation, Universität für Bodenkultur Wien (BOKU)Google Scholar
  38. Kirisits T (2004) Fungal associates of European bark beetles with emphasis on the Ophiostomatoid fungi. In: Lieutier F, Day KR, Battisti A, Grégoire J-C, Evans H (eds) Bark and wood boring insects in living trees in Europe, a synthesis. Kluwer Academic Publishers, Dordrecht, pp 181–235CrossRefGoogle Scholar
  39. Kirisits T (2010) Fungi isolated from Picea abies infested by the bark beetle Ips typographus in the Białowieża forest in north-eastern Poland. For Pathol 40:100–110. doi: 10.1111/j.1439-0329.2009.00613.x Google Scholar
  40. Kirisits T (2013) Dutch elm disease and other Ophiostoma diseases. In: Gonthier P, Nicolotti G (eds) Infectious forest diseases. CABI, Wallingford, pp 256–282CrossRefGoogle Scholar
  41. Kirisits T, Grubelnik R, Führer E (2000) Die ökologische Bedeutung von Bläuepilzen für rindenbrütende Borkenkäfer. In: Müller F (ed) Mariabrunner Waldbautage 1999. Umbau sekundärer Nadelwälder. FBVA- Berichte, Schriftenreihe der Forstlichen Bundesversuchsanstalt, Wien, vol 111, pp. 117–137. Accessed Nov 2015
  42. Kirisits T, Konrad H, Wingfield MJ, Chhetri DB (2013) Ophiostomatoid fungi associated with the Eastern Himalayan spruce bark beetle, Ips schmutzenhoferi, in Bhutan and their pathogenicity to Picea spinulosa and Pinus wallichiana. In: Seifert KA, De Beer ZW, Wingfield MJ (eds) Ophiostomatoid fungi: expanding frontiers. CBS Biodivers Ser 12:99–112Google Scholar
  43. Kirschner R (1998) Diversität mit Borkenkäfern azzoziierter filamentöser Mikropilze. Dissertation, Eberhard-Karls-Universtität, TübingenGoogle Scholar
  44. Kirschner R (2001) Diversity of filamentous fungi in bark beetle galleries in Central Europe. In: Misra JK, Horn BW (eds) Trichomyces and other fungal groups. Robert W. Lichtwardt Commemoration Volume. Science Publishers Inc, Enfield, pp 175–196Google Scholar
  45. Krehan H (2011) Borkenkäferprobleme bei Kiefern in einem Steinschlagschutzwald in Kärnten. Forstschutz Aktuell 53:2–4. Accessed Nov 2015
  46. Lieutier F, Yart A, Garcia J, Ham MC, Morelet M, Levieux J (1989) Champignons phytopathogènes associés à deux coléeoptères scolytidae du pin sylvestre (Pinus sylvestris L.) et étude préliminaire de leur agressivité envers l’hote. Ann Sci For 46:201–216CrossRefGoogle Scholar
  47. Lieutier F, Garcia J, Yart A, Vouland G, Pettinetti M, Morelet M (1991) Ophiostomatales (Ascomycetes) associated with Ips acuminatus Gyll. (Coleoptera, Scolytidae) in Scots pine (Pinus sylvestris L.) in South-Eastern France, and comparison with Ips sexdentatus Boern. Agronomie 11:807–817 (in French) CrossRefGoogle Scholar
  48. Linnakoski R (2011) Bark beetle-associated fungi in Fennoscandia with special emphasis on species of Ophiostoma and Grosmannia. Dissertationes Forestales 119. doi: 10.14214/df.119
  49. Linnakoski R, De Beer ZW, Rousi M, Niemelä P, Pappinen A, Wingfield MJ (2008) Fungi, including Ophiostoma karelicum sp. nov., associated with Scolytus ratzeburgi infesting birch in Finland and Russia. Mycol Res 112:1475–1488. doi: 10.1016/j.mycres.2008.06.007 CrossRefPubMedGoogle Scholar
  50. Linnakoski R, De Beer ZW, Rousi M, Solheim H, Wingfield MJ (2009) Ophiostoma denticiliatum sp. nov. and other Ophiostoma species associated with the birch bark beetle in southern Norway. Persoonia 23:9–15. doi: 10.3767/003158509X46803 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Linnakoski R, De Beer ZW, Ahtiainen J, Sidorov E, Niemelä P, Pappinen A, Wingfield MJ (2010) Ophiostoma spp. associated with pine- and spruce-infesting bark beetles in Finland and Russia. Persoonia 25:72–93. doi: 10.3767/003158510X550845 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Marincowitz S, Duong TA, De Beer ZW, Wingfield MJ (2015) Cornuvesica: a little known mycophilic genus with a unique biology and unexpected new species. Fungal Biol 119:615–630. doi: 10.1016/j.funbio.2015.03.007 CrossRefPubMedGoogle Scholar
  53. Masuya H, Yamaoka Y, Wingfield MJ (2013) Ophiostomatoid fungi and their associations with bark beetles in Japan. In: Seifert KA, De Beer ZW, Wingfield MJ (eds) Ophiostomatoid fungi: expanding frontiers. CBS Biodivers Ser 12:77–90Google Scholar
  54. Mathiesen A (1950) Über einige mit Borkenkäfern assoziierte Bläuepilze in Schweden. Oikos 2:275–308CrossRefGoogle Scholar
  55. Mathiesen A (1951) Einige neue Ophiostoma-Arten in Schweden. Sven Bot Tidskr 45:203–232Google Scholar
  56. Mathiesen-Käärik A (1953) Eine Übersicht über die gewöhnlichsten mit Borkenkäfern assoziierten Bläuepilze in Schweden und einige für Schweden neue Bläupilze. Medd Statens Skogsforskningsinst 43:1–74Google Scholar
  57. Mathiesen-Käärik A (1960) Studies on the ecology, taxonomy and physiology of Swedish insect-associated blue stain fungi, especially the genus Ceratocystis. Oikos 11:1–25CrossRefGoogle Scholar
  58. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Sciences Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans, LA, USA, pp 1–8Google Scholar
  59. Musvuugwa T, De Beer ZW, Duong TA, Dreyer LL, Oberlander KC, Roets F (2015) New species of Ophiostomatales from Scolytinae and Platypodinae beetles in the Cape Floristic Region, including the discovery of the sexual state of Raffaelea. Antonie van Leeuwenhoek J Microb 108:933–950. doi: 10.1007/s10482-015-0547-7 CrossRefGoogle Scholar
  60. Nylander JAA (2004) MrModeltest v.2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, SwedenGoogle Scholar
  61. O’Donnel K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7:103–116. doi: 10.1006/mpev.1996.0376 CrossRefGoogle Scholar
  62. O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. PNAS 95:2044–2049CrossRefPubMedPubMedCentralGoogle Scholar
  63. Okada G, Seifert KA, Takematsu A, Yamaoka Y (1998) A molecular phylogenetic reappraisal of the Graphium complex based on 18S rDNA sequences. Can J Bot 76:1495–1506. doi: 10.1139/b98-089 Google Scholar
  64. Pashenova NV, Vetrova VP, Matrenina RM, Sorokina EN (1995) Ophiostoma fungi in the galleries of the larch bark beetle. Lesovedenie 6:62–68Google Scholar
  65. Pattengale ND, Alipour M, Bininda-Emonds OR, Moret BM, Stamakis A (2010) How many bootstrap replicates are necessary? J Comput Biol 17:337–354. doi: 10.1089/cmb.2009.0179 CrossRefPubMedGoogle Scholar
  66. Rassi P, Hyvärinen E, Juslén A, Mannerkoski I (eds) (2010) The 2010 red list of Finnish species. Ympäristöministeriö & Suomen ympäristökeskus, HelsinkiGoogle Scholar
  67. Rebetez M, Dobbertin M (2004) Climate change may already threaten Scots pine stands in the Swiss Alps. Theor Appl Climatol 79:1–9. doi: 10.1007/s00704-004-0058-3 CrossRefGoogle Scholar
  68. Redfern DB, Stoakley JT, Steele H, Minter DW (1987) Dieback and death of larch caused by Ceratocystis laricicola sp. nov. following attack by Ips cembrae. Plant Pathol 36:467–480CrossRefGoogle Scholar
  69. Rennerfelt E (1950) Über den Zusammenhang zwischen dem Verblauen des Holzes und den Insekten. Oikos 2:120–137CrossRefGoogle Scholar
  70. Repe A, Kirisits T, Piškur B, de Groot M, Kump B, Jurc M (2013) Ophiostomatoid fungi associated with three spruce-infesting bark beetles in Slovenia. Ann For Sci 70:717–727. doi: 10.1007/s13595-013-0311-y CrossRefGoogle Scholar
  71. Robert V, Vu D, Amor AB, van de Wiele N, Brouwer C, Jabas B, Szoke S, Dridi A, Triki M, Ben Daoud S, Chouchen O, Vaas L, de Cock A, Stalpers JA, Stalpers D, Verkley GJ, Groenewald M, Dos Santos FB, Stegehuis G, Li W, Wu L, Zhang R, Ma J, Zhou M, Gorjon SP, Eurwilaichitr L, Ingsriswang S, Hansen K, Schoch C, Robbertse B, Irinyi L, Meyer W, Cardinali G, Hawksworth DL, Taylor JW, Crous PW (2013) MycoBank gearing up for new horizons. IMA Fungus 4:371–379. doi: 10.5598/imafungus.2013.04.02.16 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi: 10.1093/bioinformatics/btg180 CrossRefPubMedGoogle Scholar
  73. Sallé A, Monclus R, Yart A, Garcia J, Romary P, Lieutier F (2005) Fungal flora associated with Ips typographus: frequency, virulence, and ability to stimulate the host defence reaction in relation to insect population levels. Can J For Res 35:365–373CrossRefGoogle Scholar
  74. Seifert KA, De Beer ZW, Wingfield MJ (eds) (2013) Ophiostomatoid fungi: expanding frontiers. Utrecht, CBS-KNAW Fungal Biodiversity Centre. CBS Biodiversity Series 12Google Scholar
  75. Siitonen J (2014) Ips acuminatus kills pines in southern Finland. Silva Fenn 48: article id 1145. doi: 10.14214/sf.1145
  76. Solheim H (1986) Species of Ophiostomataceae isolated from Picea abies infested by the bark beetle Ips typographus. Nord J Bot 6:199–207CrossRefGoogle Scholar
  77. Solheim H (1992) The early stages of fungal invasion in Norway spruce infested by the bark beetle Ips typographus. Can J Bot 70:1–5. doi: 10.1139/b92-001 CrossRefGoogle Scholar
  78. Solheim H (1993) Fungi associated with the spruce bark beetle Ips typographus in an endemic area in Norway. Scan J For Res 8:118–122. doi: 10.1080/02827589309382760 CrossRefGoogle Scholar
  79. Stamakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. doi: 10.1093/bioinformatics/btu033 CrossRefGoogle Scholar
  80. Stamakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 57:758–771. doi: 10.1080/10635150802429642 CrossRefGoogle Scholar
  81. Stauffer C, Kirisits T, Nussbaumer C, Pavlin R, Wingfield MJ (2001) Phylogenetic relationships between the European and Asian eight spined larch bark beetle populations (Coleoptera, Scolytidae) inferred from DNA sequences and fungal associates. Eur J Entomol 98:99–105CrossRefGoogle Scholar
  82. Swofford DL (2002) PAUP* 4.0: phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, SunderlandGoogle Scholar
  83. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi: 10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Upadhyay HP (1981) A monograph of Ceratocystis and Ceratocystiopsis. The University of Georgia Press, GeorgiaGoogle Scholar
  85. Viiri H (1997) Fungal associates of the spruce bark beetle Ips typographus L. (Col. Scolytidae) in relation to different trapping methods. J Appl Entomol 121:529–533CrossRefGoogle Scholar
  86. Viiri H, Lieutier F (2004) Ophiostomatoid fungi associated with the spruce bark beetle, Ips typographus, in three areas in France. Ann For Sci 61:1–5CrossRefGoogle Scholar
  87. Villari C (2012) Fungi associated with the pine engraver beetle Ips acuminatus and their interactions with the host tree. Dissertation, Dipartimento di Agronomia Animali Alimenti Risorse Naturali e Ambiente, Universita’ Degli Studi Di PadovaGoogle Scholar
  88. Villari C, Battisti A, Chakraborty S, Michelozzi M, Bonello P, Faccoli M (2012) Nutritional and pathogenic fungi associated with the pine engraver beetle trigger comparable defenses in Scots pine. Tree Physiol 37:867–879. doi: 10.1093/treephys/tps056 CrossRefGoogle Scholar
  89. Villari C, Tomlinson JA, Battisti A, Boonham N, Capretti P, Massimo F (2013) Use of loop-mediated isothermal amplification for detection of Ophiostoma clavatum, the primary blue stain fungus associated with Ips acuminatus. Appl Environ Microbiol 79:2527–2533. doi: 10.1128/AEM.03612-12 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Voolma K, Mandelshtam MJ, Shcherbakov AN, Yakovlev EB, Õunap H, Süda I, Popovichev BG, Sharapa TV, Galasjeva TV, Khairetdinov RR, Lipatkin VA, Mozolevskaya EG (2004) Distribution and spread of bark beetles (Coleoptera: Scolytidae) around the Gulf of Finland: a comparative study with notes on rare species of Estonia, Finland and North-Western Russia. Entomol Fenn 15:198–210Google Scholar
  91. Wermelinger B, Rigling A, Schneider Mathis D, Dobbertin M (2008) Assessing the role of bark- and wood-boring insects in the decline of Scots pine (Pinus sylvestris) in the Swiss Rhone valley. Ecol Entomol 33:239–249. doi: 10.1111/j.1365-2311.2007.00960.x CrossRefGoogle Scholar
  92. 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, San Diego, pp 315–321Google Scholar
  93. Wingfield MJ, Seifert KA, Webber JF (eds) (1993) Ceratocystis and Ophiostoma: taxonomy, ecology and pathogenicity. APS Press, St PaulGoogle Scholar
  94. Yamaoka Y, Wingfield MJ, Takahashi I, Solheim H (1997) Ophiostomatoid fungi associated with the spruce bark beetle Ips typographus f. japonicus in Japan. Mycol Res 101:1214–1227CrossRefGoogle Scholar
  95. Yamaoka Y, Wingfield MJ, Ohsawa M, Kuroda Y (1998) Ophiostomatoid fungi associated with Ips cembrae in Japan and their pathogenicity to Japanese larch. Mycoscience 39:367–378CrossRefGoogle Scholar
  96. Yamaoka Y, Chung W-H, Masuya H, Hizai M (2009) Constant association of ophiostomatoid fungi with the bark beetle Ips subelongatus invading Japanese larch logs. Mycoscience 50:165–172CrossRefGoogle Scholar
  97. Yin M, Duong TA, Wingfield MJ, Zhou X, De Beer ZW (2015) Taxonomy and phylogeny of the Leptographium procerum complex, including Leptographium sinense sp. nov. and Leptographium longiconidiophorum sp. nov. Antonie van Leeuwenhoek J Microb 107:547–563. doi: 10.1007/s10482-014-0351-9 CrossRefGoogle Scholar
  98. Zipfel RD, De Beer ZW, Jacobs K, Wingfield BD, Wingfield MJ (2006) Multi-gene phylogenies define Ceratocystiopsis and Grosmannia distinct from Ophiostoma. Stud Mycol 55:75–97. doi: 10.3114/sim.55.1.133 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Forest SciencesUniversity of HelsinkiHelsinkiFinland
  2. 2.Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute (FABI)University of PretoriaPretoriaSouth Africa
  3. 3.Department of Forest Pathology, Mycology and Tree Physiology, Institute of Forest Ecosystem ProtectionUniversity of Agriculture in KrakówKrakówPoland
  4. 4.Department of Plant PathologyOhio State UniversityColumbusUSA
  5. 5.Dipartimento di Agronomia Animali Alimenti Risorse Naturali e AmbienteUniversità di Padova, AgripolisLegnaroItaly
  6. 6.Department of Forest and Soil Sciences, Institute of Forest Entomology, Forest Pathology and Forest Protection (IFFF)University of Natural Resources and Life Sciences, Vienna (BOKU)ViennaAustria
  7. 7.Norwegian Institute of Bioeconomy ResearchÅsNorway

Personalised recommendations