Eur. J. Entomol. 114: 77-85, 2017 | DOI: 10.14411/eje.2017.011

Fungi associated with Ips acuminatus (Coleoptera: Curculionidae) in Ukraine with a special emphasis on pathogenicity of ophiostomatoid speciesOriginal article

Kateryna DAVYDENKO1,2, Rimvydas VASAITIS2, Audrius MENKIS2
1 Ukrainian Research Institute of Forestry & Forest Melioration, Pushkinska st. 86, 61024 Kharkiv, Ukraine; e-mail: kateryna.davydenko74@gmail.com
2 Department of Forest Mycology and Plant Pathology, Uppsala BioCenter, Swedish University of Agricultural Sciences, P.O. Box 7026, SE-75007, Uppsala, Sweden; e-mails: rimvys.vasaitis@slu.se, audrius.menkis@slu.se

Conifer bark beetles are well known to be associated with fungal complexes, which consist of pathogenic ophiostomatoid fungi as well as obligate saprotroph species. However, there is little information on fungi associated with Ips acuminatus in central and eastern Europe. The aim of the study was to investigate the composition of the fungal communities associated with the pine engraver beetle, I. acuminatus, in the forest-steppe zone in Ukraine and to evaluate the pathogenicity of six associated ophiostomatoid species by inoculating three-year-old Scots pine seedlings with these fungi. In total, 384 adult beetles were collected from under the bark of declining and dead Scots pine trees at two different sites. Fungal culturing from 192 beetles resulted in 447 cultures and direct sequencing of ITS rRNA from 192 beetles in 496 high-quality sequences. Identification of the above revealed that the overall fungal community was composed of 60 species. Among these, the most common were Entomocorticium sp. (24.5%), Diplodia pinea (24.0%), Ophiostoma ips (16.7%), Sydowia polyspora (15.1%), Graphilbum cf rectangulosporium (15.1%), Ophiostoma minus (13.8%) and Cladosporium pini-ponderosae (13.0%). Pathogenicity tests were done using six species of ophiostomatoid fungi, which were inoculated into Scots pine seedlings. All ophiostomatoid fungi tested successfully infected seedlings of Scots pine with varying degrees of virulence. Ophiostoma minus was the only fungus that caused dieback in inoculated seedlings. It is concluded that I. acuminatus vectors a species-rich fungal community including pathogens such as D. pinea and O. minus. The fungal community reported in the present study is different from that reported in other regions of Europe. Pathogenicity tests showed that O. minus was the most virulent causing dieback in seedlings of Scots pine, while other fungi tested appeared to be only slightly pathogenic or completely non-pathogenic.

Keywords: Coleoptera, Curculionidae, pine engraver beetle, Scots pine, Ips acuminatus, pathogens, Ophiostoma, Diplodia pinea, insect-fungus interaction

Received: March 15, 2016; Revised: December 28, 2016; Accepted: December 28, 2016; Published online: January 30, 2017  Show citation

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DAVYDENKO, K., VASAITIS, R., & MENKIS, A. (2017). Fungi associated with Ips acuminatus (Coleoptera: Curculionidae) in Ukraine with a special emphasis on pathogenicity of ophiostomatoid species. EJE, 114, Article 77-85. https://doi.org/10.14411/eje.2017.011
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    References

    1. Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D. J. 1990: Basic local alignment search tool. - J. Mol. Biol. 215: 403-410. Go to original source...
    2. Camargo J. 1993: Must dominance increase with the number of subordinate species in competitive interactions? - J. Theor. Biol. 161: 537-542. Go to original source...
    3. Colombari F., Battisti A., Schroeder L.M. & 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. Forest Res. 131: 553-561. Go to original source...
    4. Christiansen E. & Bakke A. 1988: The spruce bark beetle of Eurasia. In Berryman A. (ed.): Dynamics of Forest Insect Populations. Plenum, New York, pp. 480-503. Go to original source...
    5. 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. Go to original source...
    6. De Beer Z.W. & Wingfield M.J. 2013: Emerging lineages in the Ophiostomatales. In Seifert K.A., de Beer Z.W. & Wingfield M.J. (eds): The Ophiostomatoid Fungi: Expanding Frontiers. Vol. 12. CBS, Utrecht, pp. 21-46.
    7. De Beer Z.W., Seifert K. & Wingfield M. 2013: A nomenclator for ophiostomatoid genera and species in the Ophiostomatales and Microascales. In Seifert K.A., de Beer Z.W. & Wingfield M.J. (eds): The Ophiostomatoid Fungi: Expanding Frontiers. Vol. 12. CBS, Utrecht, pp. 245-322.
    8. De Beer Z.W., Duong T.A., Barnes I., Wingfield B.D. & Wingfield M.J. 2014: Redefining Ceratocystis and allied genera. - Studies Mycol. 79: 187-219. Go to original source...
    9. Dori-Bachash M., Avrahami-Moyal L., Protasov A., Mendel Z. & Freeman S. 2015: The occurrence and pathogenicity of Geosmithia spp. and common blue-stain fungi associated with pine bark beetles in planted forests in Israel. - Eur. J. Plant Pathol. 143: 627-639. Go to original source...
    10. Francke-Grosmann H. 1952: Über die Ambrosiazucht der beiden Kiefernborkenkäfer Myelophilus minor Htg. und Ips acuminatus Gyll. - Medd. St. Skogsforskningsinst. 41: 1-52.
    11. Francke-Grosmann H. 1963: Die Übertragung der Pilzflora bei dem Borkenkäfer Ips acuminatus Gyll.: Ein Beitrag zur Kenntnis der Ipiden-Symbiosen. - J. Appl. Entomol. 52: 355-361. Go to original source...
    12. Gardes M. & Bruns T.D. 1993: Its primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. - Mol. Ecol. 2: 113-118. Go to original source...
    13. Glass N.L. & Donaldson G.C. 1995: Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. - Appl. Environ. Microbiol. 61: 1323-1330. Go to original source...
    14. Goldazarena A., Romón P. & López S. 2012: Bark beetles control in forests of Northern Spain. In Larramendy M.L. & Soloneski S. (eds): Integrated Pest Management and Pest Control - Current and Future Tactics. InTech, Open Access Publisher, pp. 323-352. Go to original source...
    15. 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. Forest Sci. 57: 681-690. Go to original source...
    16. Harrington T.C. & Wingfield M.J. 1998: The Ceratocystis species on conifers. - Can. J. Bot. 76: 1446-1457. Go to original source...
    17. Jacobs K., Bergdahl D.R., Wingfield M.J., Halik S., Seifert K.A., Bright D.E. & Wingfield B.D. 2004: Leptographium wingfieldii introduced into North America and found associated with exotic Tomicus piniperda and native bark beetles. - Mycol. Res. 108: 411-418. Go to original source...
    18. Jankowiak R. 2006: Fungi associated with Tomicus piniperda in Poland and assessment of their virulence using Scots pine seedlings. - Ann. Forest Sci. 63: 801-808. Go to original source...
    19. Jankowiak R. 2012: Ophiostomatoid fungi associated with Ips sexdentatus on Pinus sylvestris in Poland. - Dendrobiology 68: 43-53.
    20. Jankowiak R. 2013: Assessing the virulence of ophiostomatoid fungi associated with the pine-infesting weevils to scots pine Pinus sylvestris L. seedlings. - Acta Agrobot. 66: 85-94. Go to original source...
    21. Jankowiak R. & Bilañski P. 2007: Fungal flora associated with Tomicus piniperda L. in an area close to a timber yard in southern Poland. - J. Appl. Entomol. 131: 579-584. Go to original source...
    22. Jankowiak R. & Bilanski P. 2013: Ophiostomatoid fungi associated with root-feeding bark beetles on Scots pine in Poland. - Forest Pathol. 43: 422-428. Go to original source...
    23. Jankowiak R. & Kolaøík M. 2010: Fungi associated with the fir bark beetle Cryphalus piceae in Poland. - Forest Pathol. 40: 133-144. Go to original source...
    24. Jankowiak R., Kolaøík M. & Bilañski P. 2014: Association of Geosmithia fungi (Ascomycota: Hypocreales) with pine-and spruce-infesting bark beetles in Poland. - Fungal Ecol. 11: 71-79. Go to original source...
    25. Kaarik A. 1975: Succession of microorganisms during wood decay. In Liese W. (ed.): Biological Transformation of Wood by Microorganisms. Proceedings of the Sessions on Wood Products Pathology at the 2nd International Congress of Plant Pathology September 10-12, 1973, Minneapolis, USA. Springer, Berlin, Heidelberg, New York, pp. 39-51.
    26. Kim J.J., Kim S.H., Lee S. & Breuil C. 2003: Distinguishing Ophiostoma ips and Ophiostoma montium, two bark beetle-associated sapstain fungi. - FEMS Microbiol. Lett. 222: 187-192. Go to original source...
    27. Kirisits T. 2004: Fungal associates of European bark beetles with special emphasis on the ophiostomatoid fungi. In Lieutier F., Day K.R., Battisti A., Grégoire J.-C. & Evans H.F. (eds): Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis. Springer, Dordrecht, pp. 181-236. Go to original source...
    28. Kirisits T. 2010: Fungi isolated from Picea abies infested by the bark beetle Ips typographus in the Bialowieza forest in north-eastern Poland. - Forest Pathol. 40: 100-110. Go to original source...
    29. Kirisits T. 2013: Dutch elm disease and other Ophiostoma diseases. In Gonthier P. & Nicolotti G. (eds): Infectious Forest Diseases. CABI, Wallingford, pp. 256-282. Go to original source...
    30. Klepzig K.D., Flores-Otero J., Hofstetter R.W. & Ayres M.P. 2004: Effects of available water on growth and competition of southern pine beetle associated fungi. - Mycol. Res. 108: 183-188. Go to original source...
    31. Kolaøík 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. Go to original source...
    32. Kolaøík M., Kubátová A., Hulcr J. & Pa¾outová 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. Go to original source...
    33. Krokene P. & Solheim H. 1998: Pathogenicity of four blue-stain fungi associated with aggressive and nonaggressive bark beetles. - Phytopathology 88: 39-44. Go to original source...
    34. Långström B., Solheim H., Hellqvist C. & Gref R. 1993: Effects of pruning young Scots pines on host vigour and susceptibility to Leptographium wingfieldii and Ophiostoma minus, two blue-stain fungi associated with Tomicus piniperda. - Eur. J. Forest Pathol. 23: 400-415. Go to original source...
    35. 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. Go to original source...
    36. Lieutier F., Yart A. & Salle A. 2009: Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers. - Ann. Forest Sci. 66: 801, 22 pp. Go to original source...
    37. Linnakoski R. 2011: Bark Beetle-Associated Fungi in Fennoscandia with Special Emphasis on Species of Ophiostoma and Grosmannia. Dissertationes Forestales 119. Faculty of Science and Forestry, School of Forest Sciences, University of Eastern Finland, 74 pp. Go to original source...
    38. Linnakoski R., de Beer Z.W., Ahtiainen J., Sidorov E., Niemela P., Pappinen A. & Wingfield M.J. 2010: Ophiostoma spp. associated with pine- and spruce-infesting bark beetles in Finland and Russia. - Persoonia 25: 72-93. Go to original source...
    39. Linnakoski R., De Beer Z.W., Niemelä P. & Wingfield M.J. 2012: Associations of conifer-infesting bark beetles and fungi in Fennoscandia. - Insects 3: 200-227. Go to original source...
    40. Linnakoski R., Jankowiak R., Villari C., Kirisits T., Solheim H., de Beer Z.W. & Wingfield M.J. 2016: The Ophiostoma clavatum species complex: a newly defined group in the Ophiostomatales including three novel taxa. - Antonie Van Leeuwenhoek Int. J. Gener. Mol. Microbiol. 109: 987-1018. Go to original source...
    41. Lu Q., Decock C., Zhang X.Y. & 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 Int. J. Gener. Mol. Microbiol. 96: 275-293. Go to original source...
    42. Luchi N., Mancini V., Feducci M., Santini A. & Capretti P. 2012: Leptoglossus occidentalis and Diplodia pinea: a new insect-fungus association in Mediterranean forests. - Forest Pathol. 42: 246-251. Go to original source...
    43. Magguran A.M. 1998: Ecological Diversity and its Measurement. Princeton University Press, Princeton, 192 pp.
    44. Markovskaja S., Kacergius A., Davydenko K. & Fraser S. 2016: First record of Neocatenulostroma germanicum on pines in Lithuania and Ukraine and its co-occurrence with Dothistroma spp. and other pathogens. - Forest Pathol. 46: 522-533. Go to original source...
    45. Mathiesen A. 1950: Über einige Borkenkäfern assoziierte Bläuepilze in Schweden. - Oikos 2: 275-308. Go to original source...
    46. Mathiesen A. 1951: Enige neue Ophiostoma-arten in Schweden. - Svensk Bot. Tidskr. 45: 203-232.
    47. Mathiesen-Käärik A. 1953: Eine Übersicht über die gewöhnlichsten mit Borkenkäfern assoziierten Bläuepilze in Schweden und einige für Schweden neue Bläupilze. - Medd. St. Skogsforskningsinst. 43: 1-74.
    48. Mathiesen-Käärik A. 1960: Studies on the ecology, taxonomy and physiology of Swedish insect-associated blue stain fungi, especially the genus Ceratocystis. - Oikos 11: 1-25. Go to original source...
    49. Mead R. & Curnow R.N. 1983: Statistical Methods in Agriculture and Experimental Biology. Princeton University Press, Princeton, 192 pp. Go to original source...
    50. Menkis A., Vasiliauskas R., Taylor A.F.S., Stenstrom E., Stenlid J. & Finlay R. 2006: Fungi in decayed roots of conifer seedlings in forest nurseries, afforested clear-cuts and abandoned farmland. - Plant Pathol. 55: 117-129. Go to original source...
    51. Menkis A., Östbrant I.-L., Davydenko K., Bakys R., Balalaikins M. & Vasaitis R. 2016: Scolytus multistriatus associated with Dutch elm disease on the island of Gotland: phenology and communities of vectored fungi. - Mycol. Progr. 15: 55, 8 pp. Go to original source...
    52. Öhrn P. 2012: The Spruce Bark Beetle Ips typographus in a Changing Climate: Effects of Weather Conditions on the Biology of Ips typographus. Swedish University of Agricultural Sciencies, Uppsala, 27 pp.
    53. Oliva J., Boberg J. & Stenlid J. 2013: First report of Diplodia pinea on Scots pine (Pinus sylvestris) and Austrian pine (P. nigra) in Sweden. - New Dis. Rep. 27: 23. Go to original source...
    54. Ohtaka N., Masuya H., Yamaoka Y. & Kaneko S. 2006. Two new Ophiostoma species lacking conidial states isolated from bark beetles and bark beetle-infested Abies species in Japan. - Botany 84: 282-293. Go to original source...
    55. 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. Go to original source...
    56. Ploetz R.C., Hulcr J., Wingfield M.J. & de Beer Z.W. 2013: Destructive tree diseases associated with ambrosia and bark beetles: black swan events in tree pathology? - Plant Dis. 97: 856-872. Go to original source...
    57. Rennerfelt E. 1950: Über den Zusammenhang zwischen dem Verblauen des Holzes und den Insekten. - Oikos 2: 120-137. Go to original source...
    58. Romon P., Zhou X., Iturrondobeitia J.C., Wingfield M.J. & 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. Go to original source...
    59. Siitonen J. 2014: Ips acuminatus kills pines in southern Finland. - Silva Fenn. 48: 1145, 7 pp. Go to original source...
    60. Simpson E.H. 1949: Measurement of diversity. - Nature 163: 688. Go to original source...
    61. Six D.L. 2012: Ecological and evolutionary determinants of bark beetle - fungus symbioses. - Insects 3: 339-366. Go to original source...
    62. Six D.L. & Bentz B.J. 2007: Temperature determines symbiont abundance in a multipartite bark beetle-fungus ectosymbiosis. - Microb. Ecol. 54: 112-118. Go to original source...
    63. Six D.L. & Wingfield M.J. 2011: The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. - Annu. Rev. Entomol. 56: 255-272. Go to original source...
    64. Shannon C.E. 1948: A mathematical theory of communication. - The Bell Syst. Tech. J. 27: 379-423. Go to original source...
    65. Solheim H. 1988: Pathogenicity of some Ips typographus-associated blue-stain fungi to Norway spruce. - Medd. Norsk Inst. Skogforsk. 40: 14, 11 pp.
    66. Solheim H. & Krokene P. 1998: Growth and virulence of mountain pine beetle associated blue-stain fungi, Ophiostoma clavigerum and Ophiostoma montium. - Can. J. Bot. 76: 561-566. Go to original source...
    67. Solheim H., Langstrom B. & Hellqvist C. 1993: Pathogenicity of the blue-stain fungi Leptographium wingfieldii and Ophiostoma minus to Scots pine - effect of tree pruning and inoculum density. - Can. J. Forest Res. 23: 1438-1443. Go to original source...
    68. Solheim H., Krokene P. & Långström 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. Go to original source...
    69. Villari C. 2012: Fungi Associated with the Pine Engraver Beetle Ips acuminatus And their Interactions with the Host Tree. PhD Thesis, University of Padova, 142 pp.
    70. 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. 32: 867-879. Go to original source...
    71. Villari C., Tomlinson J.A., Battisti A., Boonham N., Capretti P. & Faccoli M. 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. Go to original source...
    72. Waalberg M.E. 2015. Fungi Associated with Three Common Bark Beetle Species in Norwegian Scots Pine Forest. PhD Thesis, Norwegian University of Life Sciences, 46 pp.
    73. White T.J., Bruns T.D., Lee S. & Taylor J. 1990: Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis M.A., Gelfand D.H., Sninsky J.J. & White T.J. (eds): PCR Protocols: A Guide to Methods and Applications. Academic Press, New York, pp. 315-322. Go to original source...
    74. Whitney H.S., Banoni R.J. & Oberwinkler F. 1987: Entomocorticium dendroctoni gen. et sp. nov. (Basidiomycotina), a possible nutritional symbiote of the mountain pine beetle in lodgepole pine in British Columbia. - Can. J. Bot. 65: 95-102. Go to original source...
    75. Wingfield M.J., Seifert K.A. & Webber J.F. 1993: Ceratocystis and Ophiostoma: Taxonomy, Ecology and Pathogenicity. American Phytopathological Society Press, St. Paul, 293 pp.
    76. Zhou X., Burgess T.I., De Beer Z.W., Lieutier F., Yart A., Klepzig K. & Wingfield M.J. 2007: High intercontinental migration rates and population admixture in the sapstain fungus Ophiostoma ips. - Mol. Ecol. 16: 89-99. Go to original source...

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