Skip to main content
SpringerLink
Log in

Ophiostomatoid fungi including two new fungal species associated with pine root-feeding beetles in northern Spain

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Many bark beetles live in a symbiosis with ophiostomatoid fungi but very little is known regarding these fungi in Spain. In this study, we considered the fungi associated with nine bark beetle species and one weevil infesting two native tree species (Pinus sylvestris and Pinus nigra) and one non-native (Pinus radiata) in Cantabria (Northern Spain). This included examination of 239 bark beetles or their galleries. Isolations yielded a total of 110 cultures that included 11 fungal species (five species of Leptographium sensu lato including Leptographium absconditum sp. nov., five species of Ophiostoma sensu lato including Ophiostoma cantabriense sp. nov, and one species of Graphilbum). The most commonly encountered fungal associates of the bark beetles were Grosmannia olivacea, Leptographium procerum, and Ophiostoma canum. The aggressiveness of the collected fungal species was evaluated using inoculations on two-year-old P. radiata seedlings. Leptographium wingfieldii, Leptographium guttulatum, and Ophiostoma ips were the only species capable of causing significant lesions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aghayeva DN, Wingfield MJ, De Beer ZW, Kirisits T (2004) Two new Ophiostoma species with Sporothrix anamorphs from Austria and Azerbaijan. Mycologia 96:866–878

    Article  PubMed  Google Scholar 

  • Alexander SA, Horner WE, Lewis KJ (1988) Leptographium procerum as a pathogen of pines. In: Harrington TC, Cobb F (eds) Leptographium root diseases on conifers. APS Press, St. Paul, pp 97–112

    Google Scholar 

  • Balachowsky A (1949) Coleoptera, Scolytides. Lechevalier P (ed), 50, Faune de France, Paris

  • Bueno A, Diez JJ, Fernández MM (2010) Ophiostomatoid fungi transported by Ips sexdentatus (Coleoptera; Scolytidae) in Pinus pinaster in NW Spain. Silva Fenn 44:387–397

    Article  Google Scholar 

  • Camargo JA (1993) Must dominance increase with the number of subordinate species in competitive interactions? J Theor Biol 161:537–542

    Article  Google Scholar 

  • Christiansen E, Solheim H (1990) The bark beetle-associated blue-stain fungus Ophiostoma polonicum can kill various spruces and Douglas fir. Eur J For Pathol 20:436–446

    Article  Google Scholar 

  • De Ana Magán FJF (1982) Las hogueras en el monte y el ataque del hongo Leptographium gallaeciae sp. nv. sobre P. pinaster Ait. Bol Serv Plagas 8:69–92

    Google Scholar 

  • De Ana Magán FJF (1983) Enfermedad del Pinus pinaster en Galicia Leptographium gallaeciae F. Magan sp. nov. An INIA/Ser Forestal 7:165–169

    Google Scholar 

  • De Beer ZW, Wingfield MJ (2013) Emerging lineages in the Ophiostomatales. In: Seifert KA, De Beer ZW, Wingfield MJ (eds) The ophiostomatoid fungi: expanding frontiers, CBS biodiversity series 12. CBS Press, Utrecht, pp 21–46

    Google Scholar 

  • De Beer ZW, Harrington TC, Vismer HF, Wingfield BD, Wingfield MJ (2003) Phylogeny of the Ophiostoma stenoceras–Sporothrix schenckii complex. Mycologia 95:434–441

    Article  PubMed  Google Scholar 

  • 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) The ophiostomatoid fungi: expanding frontiers, CBS biodiversity series 12. CBS Press, Utrecht, pp 243–320

    Google Scholar 

  • De Meyer EM, De Beer ZW, Summerbell RC, Moharram AM, de Hoog GS, Vismer HF, Wingfield MJ (2008) Taxonomy and phylogeny of new wood- and soil-inhabiting Sporothrix species in the Ophiostoma stenoceras-Sporothrix schenckii complex. Mycologia 100:647–661

    Article  PubMed  Google Scholar 

  • Duong TA, De Beer ZW, Wingfield BD, Wingfield MJ (2012) Phylogeny and taxonomy of species in the Grosmannia serpens complex. Mycologia 104:715–732

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenetics: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fernández MMF, García AE, Lieutier F (2004) Effects of various densities of Ophiostoma ips inoculations on Pinus sylvestris in north-western Spain. For Path 34:213–223

    Article  Google Scholar 

  • Gil L, Pajares JA (1986) Los escolitidos de las coníferas en la península ibérica. Monografías INIA n.53. MAPA. Madrid, p 194

  • 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 61:1323–1330

    PubMed  CAS  PubMed Central  Google Scholar 

  • Glez-Peña D, Gómez-Blanco D, Reboiro-Jato M, Fdez-Riverola F, Posada D (2010) ALTER: program-oriented format conversion of DNA and protein alignments. Nucleic Acids Research. Web Server issue. ISSN: 0305-1048. doi: 10.1093/nar/qkq321

  • Grüne S (1979) Handbuch zur bestimmung der europaischen Borkenkafer—brief illustrated key to European bark beetles. Schaper, Hannover

    Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2006) New algorithms and methods to estimate maximum-likehood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  Google Scholar 

  • Harrington TC, Cobb FW (1988) Leptographium root diseases on conifers. APS Press, St Paul

    Google Scholar 

  • Hill TCJ, Kerry A, Walsh JA, Harris B, Moffett F (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43:1–11

    Article  PubMed  CAS  Google Scholar 

  • Jacobs K, Wingfield MJ (2001) Leptographium species, tree pathogens, insects associates and agents of blue stain. APS Press, St. Paul

    Google Scholar 

  • Jacobs K, Wingfield MJ, Coetsee C, Kirisits T, Wingfield BD (2001) Leptographium guttulatum sp. nov., a new species from spruce and pine in Europe. Mycologia 93:380–388

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Jacobs K, Solheim H, Wingfield BD, Wingfield MJ (2005) Taxonomic re-evaluation of Leptographium lundbergii based on DNA sequence comparisons and morphology. Mycol Res 109:1141–1161

    Article  Google Scholar 

  • Jankowiak R (2006) Fungi associated with Tomicus piniperda in Poland and assessment of their virulence using Scots pine seedlings. Ann For Sci 63:801–808

    Article  Google Scholar 

  • Jankowiak R, Bilański P (2013a) Diversity of ophiostomatoid fungi associated with the large pine weevil, Hylobius abietis and infested Scots pine seedlings in Poland. Ann For Sci 70:391–402

    Article  Google Scholar 

  • Jankowiak R, Bilański P (2013b) Ophiostomatoid fungi associated with root-feeding bark beetles on Scots pine in Poland. For Path 43:422–428

    Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Ac Res 30:3059–3066

    Article  CAS  Google Scholar 

  • Kirisits T (2004) Fungal associates of European bark beetles with special emphasis on ophiostomatoid fungi. In: Lieutier F, Day KR, Battisti A, Grégoire J-C, Evans HF (eds) Bark and wood boring insects in living trees in Europe, a synthesis. Springer, Dordrecht, pp 181–236

    Chapter  Google Scholar 

  • Lackner AL, Alexander SA (1982) Occurrence and pathogenicity of Verticicladiella procera in Christmas tree plantations in Virginia. Plant Dis 66:211–212

    Article  Google Scholar 

  • Langström B, Solheim H, Hellqvist C, Krokene P (2001) Host resistance in defoliated pine: effects of single and mass inoculations using bark beetle-associated blue-stain fungi. Agric For Entomol 3:211–216

    Article  Google Scholar 

  • Lieutier F, Yart A, Garcia J, Ham MC, Morelet M, Levieux J (1989) Champignons phytopathogènes associés à deux coléoptères scolytidae du pin sylvestre (Pinus sylvestris L.) et étude préliminaire de leur agressivité envers l’hôte. Ann For Sci 46:201–216

    Article  Google Scholar 

  • Lieutier F, Yart A, Ye H, Sauvard D, Gallois V (2004) Variations in growth and virulence of Leptographium wingfieldii Morelet, a fungus associated with the bark beetle Tomicus piniperda L. Ann For Sci 61:45–53

    Article  Google Scholar 

  • López S, Romón P, Iturrondobeitia JC, Goldarazena A (2007) Los escolítidos de las coníferas del País Vasco: guía práctica para su identificación y control. ISBN 978-84-457-2650-1

  • Lu Q, Decock C, Zhang XY, Maraite H (2009) Ophiostomatoid fungi (Ascomycota) associated with Pinus tabuliformis infested by Dendroctonus valens (Coleoptera) in northern China and an assessment of their pathogenicity on mature trees. Antonie Van Leeuwenhoek 96:275–293

    Article  PubMed  Google Scholar 

  • Marimon R, Cano J, Gené J, Sutton DA, Kawasaki M, Guarro J (2007) Sporothrix brasiliensis, S. globosa, and S. mexicana, three new Sporothrix species of clinical interest. J Clin Microbiol 45:3198–3206

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Marmolejo JG, Butin H (1990) New conifer-inhabiting species of Ophiostoma and Ceratocystiopsis (Ascomycetes, Microascales) from Mexico. Sydowia 42:193–199

    Google Scholar 

  • Mathiesen A (1950) Über einige mit Borkenkäfern assoziierten Bläuepilze in Schweden. Oikos 2:275–308

    Article  Google Scholar 

  • Mathiesen-Käärik A (1953) Eine Übersicht über die gewöhnlichsten mit Borkenkäfern assoziierten Bläuepilze in Schweden und einige für Schweden neue Bläuepilze. Meddn St Skogforsk 43:1–74

    Google Scholar 

  • O’Donnell K (2000) Molecular phylogeny of the Nectria haematococca-Fusarium solani species complex. Mycologia 92:919–938

    Article  Google Scholar 

  • Owen DR, Lindahl KQ Jr, Wood DL, Parmeter JR Jr (1987) Pathogenicity of fungi isolated from Dendroctonus valens, D. brevicomis, and D. ponderosae to ponderosa pine seedlings. Phytopathology 77:631–636

    Article  Google Scholar 

  • Parmeter JRJr, Slaughter GW, Chen MM, Wood DL, Stubbs HA (1989) Single and mixed inoculations of ponderosa pine with fungal associates of Dendroctonus spp. Phytopathology 79:786–792

    Article  Google Scholar 

  • Pestaña M, Santolamazza-Carbone S (2010) Mutual benefit interactions between banded pine weevil Pissodes castaneus and blue-stain fungus Leptographium serpens in maritime pine. Agric For Entomol 12:371–379

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Raffa KF, Smalley EB (1988) Response of red and jack pines to inoculations with microbial associates of the pine engraver, Ips pini (Coleoptera: scolytidae). Can J For Res 18:581–586

    Article  Google Scholar 

  • 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 36:467–480

    Article  Google Scholar 

  • Roets F, De Beer ZW, Wingfield MJ, Crous PW, Dreyer LL (2008) Ophiostoma gemellus and Sporothrix variecibatus from mites infesting Protea infructescences in South Africa. Mycologia 100:496–510

    Article  PubMed  Google Scholar 

  • Roets F, Wingfield BD, De Beer ZW, Wingfield MJ, Dreyer LL (2010) Two new Ophiostoma species from Protea caffra in Zambia. Persoonia 24:18–28

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Romón P, Zhou XD, Iturrondobeitia JC, Wingfield MJ, Goldarazena A (2007) Ophiostoma species (Ascomycetes: ophiostomatales) associated with bark beetles (Coleoptera: Scolytinae) colonizing Pinus radiata in northern Spain. Can J Microbiol 53:756–767

    Article  PubMed  Google Scholar 

  • Romón P, De Beer ZW, Zhou XD, Duong TA, Wingfield BD, Wingfield MJ (2014) Multigene phylogenies of ophiostomataceae ascomycetes associated with Monterey pine bark beetles in Spain reveal three new fungal species. Mycologia 106:119–132

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Seifert KA (1993) Sapstain of commercial lumber by species of Ophiostoma and Ceratocystis. In: Wingfield MJ, Seifert KA, Webber JF (eds) Ceratocystis and Ophiostoma: taxonomy, ecology, and pathogenicity. APS Press, St Paul, pp 141–151

    Google Scholar 

  • Six DL, Wingfield MJ (2011) The role of phytopathogenicity in bark beetle–fungus symbioses: a challenge to the classic paradigm. Ann Rev Entomol 56:255–272

    Article  CAS  Google Scholar 

  • Solheim H, Krokene P, Langström B (2001) Effects of growth and virulence of associated blue-stain fungi on host colonization behaviour of the pine shoot beetles Tomicus minor and T. piniperda. Plant Pathol 50:111–116

    Article  Google Scholar 

  • Swofford DL (2003) PAUP (Phylogenetic Analysis Using Parsimony), version 4.0b10. Sinauer Associates, Massachusetts

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Villarreal M, Rubio V, De Troya MT, Arenal F (2005) A new Ophiostoma species isolated from Pinus pinaster in the Iberian Peninsula. Mycotaxon 92:259–268

    Google Scholar 

  • 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 application. Academic Press, New York, pp 315–322

    Chapter  Google Scholar 

  • Wingfield MJ, Gibbs JN (1991) Leptographium and Graphium species associated with pine-infesting bark beetles in England. Mycol Res 95:1257–1260

    Article  Google Scholar 

  • Yamaoka Y, Swanson RH, Hiratsuka Y (1990) Inoculation of lodgepole pine with four blue-stain fungi associated with mountain pine beetle, monitored by a heat pulse velocity (HPV) instrument. Can J For Res 20:31–36

    Article  Google Scholar 

  • 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 101:1215–1227

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge the University of Pretoria, the National Research Foundation of South Africa (NRF), the Department of Education, Universities and Research of Basque Government, members of Tree Protection Co-operative Programme (TPCP), and the NRF/DST Centre of Excellence in Tree Health Biotechnology (CTHB) for financial support. We also acknowledge the technical and logistical support of Ms. Milagros Vallejo of the Cantabria Government and Ms. Izette Greyling, Mr. Darryl Herron and Mr. Johan van der Linde of the Forestry and Agricultural Biotechnology Institute (FABI).

Author information

Authors and Affiliations

  1. Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0002, South Africa

    Pedro Romón & Brenda D. Wingfield

  2. Department of Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0002, South Africa

    Z. Wilhelm De Beer & Michael J. Wingfield

  3. Department of Agroforestry Sciences, University of Valladolid, ETSIIAA Palencia, Avda. Madrid 57, 34071, Palencia, Spain

    Mercedes Fernández

  4. Department of Plant Production and Forest Resources, University of Valladolid, ETSIIAA Palencia, Avda. Madrid 57, 34071, Palencia, Spain

    Julio Diez

Authors
  1. Pedro Romón
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Z. Wilhelm De Beer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mercedes Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julio Diez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Brenda D. Wingfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael J. Wingfield
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pedro Romón.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romón, P., De Beer, Z.W., Fernández, M. et al. Ophiostomatoid fungi including two new fungal species associated with pine root-feeding beetles in northern Spain. Antonie van Leeuwenhoek 106, 1167–1184 (2014). https://doi.org/10.1007/s10482-014-0286-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-014-0286-1

Keywords

Search

Navigation