Characterization of fungal communities associated with the bark beetle Ips typographus varies depending on detection method, location, and beetle population levels

Mycological Progress

Volumn 12, Issue 1, 2013, Pages 127-140

  Giordano, Luana ^a   Garbelotto, Matteo ^b   Nicolotti, Giovanni ^a   Gonthier, Paolo ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Culture isolation; DNA cloning; Environmental sequencing; Fungal diversity; Ophiostomatoid fungi; Picea abies

Indexed keywords

BASIDIOMYCOTA; COLEOPTERA; FUNGI; HEXAPODA; IPS TYPOGRAPHUS; OPHIOSTOMA; OPHIOSTOMA BICOLOR; OTUS; PICEA; PICEA ABIES; SCOLYTINAE;

EID: 84872594395     PISSN: 1617416X     EISSN: 18618952     Source Type: Journal    
DOI: 10.1007/s11557-012-0822-1     Document Type: Article

References (78)

1. Allen TR, Millar T, Berch SM, Berbee ML (2003) Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol 160: 255-272.
2. Aukema BH, Werner RA, Haberkern KE, Illman BL, Clayton MK, Raffa KF (2005) Quantifying sources of variation in the frequency of fungi associated with spruce beetles: implications for hypothesis testing and sampling methodology in bark beetle-symbiont relationships. For Ecol Manag 217: 187-202.
3. 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.
4. Christiansen E, Bakke A (1988) The spruce bark beetle of Eurasia. In: Berryman AA (ed) Dynamics of Forest Insect Populations. Pattern, Causes, Implications. Plenum Press, New York and London, pp 479-503.
5. 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.
6. Chung WH, Kim JJ, Yamaoka Y, Uzunovic A, Masuya H, Breuil C (2006) Ophiostoma breviusculum sp. nov. (Ophiostomatales, Ascomycota) is a new species in the Ophiostoma piceae complex associated with bark beetles infesting larch in Japan. Mycologia 98: 801-814.
7. Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol-UK 5: 3-21.
8. Domsch KH, Gams W, Anderson TH (1980) Compendium of soil fungi. Academic Press, London.
9. EstimateS 8. 2. 0 (2009) By Robert Colwell, University of Connecticut, Storrs, Connecticut.
10. Faccoli M, Stergulc F (2004) Ips typographus (L.) pheromone trapping in south Alps: spring catches determine damage thresholds. J Appl Entomol 128: 307-311.
11. Fisher PJ, Petrini O, Petrini LE (1991) Endophytic ascomycetes and deuteromycetes in roots of Pinus sylvestris. Nova Hedwigia 52: 11-15.
12. Francke-Grosmann H (1956) Hautdrüsen als Trager der Pilzsymbiose bei Ambrosiakäfern. Z Morph u Ökol Tiere 45: 275-308.
13. Frigimelica G, Stergulc F, Faccoli M, Battisti A (2000) A comparison of damage caused by fungi and insects in pure and mixed stands of Picea abies in the south-eastern Italian Alps. In: Hasenauer H. (ed) Proceedings of the International Conference Forest ecosystem restoration. ecological and economical impacts of restoration processes in secondary coniferous forests. Vienna, Austria, pp 85-91.
14. Furniss MM, Solheim H, Christiansen E (1990) Transmission of blue-stain fungi by Ips typographus (Coleoptera: Scolytidae) in Norway spruce. Ann Entomol Soc Am 83: 712-716.
15. Grosmann H (1931) Beiträge zur Kenntnis der Lebensgemeinschaft zwischen Borkenkäfern und Pilzen. Z Parasitenk 3: 56-102.
16. Harrington TC, Furniss MM, Shaw CG (1981) Dissemination of Hymenomycetes by Dendroctonus pseudotsugae (Coleoptera: Scolytidae). Phytopathology 71: 551-554.
17. 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: 37-55.
18. 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.
19. Jankowiak R, Hilszczański J (2005) Ophiostomatoid fungi associated with Ips typographus (L.) on Picea abies (L.) H. Karst. and Pinus sylvestris L. in North-Eastern Poland. Acta Soc Bot Pol 74: 345-350.
20. Jankowiak R, Rossa R (2008) Associations between Pityogenes bidentatus and fungi in young managed Scots pine stands in Poland. For Pathol 38: 169-177.
21. Juzwik J, French DW (1983) Ceratocystis fagacearum and Ceratocystis piceae on the surface of free-flying and fungus-mat-inhabiting nitidulids. Phytopathology 73: 1164-1168.
22. Kautz M, Dworschak K, Gruppe A, Schopf R (2011) Quantifying spatio-temporal dispersion of bark beetle infestations in epidemic and non-epidemic conditions. For Ecol Manag 262: 598-608.
23. Kiffer E, Morelet M (1997) Les deutéromycètes. Classification et clés d'identification générique. INRA Editions, Paris.
24. Kim JJ, Allen EA, Humble LM, Breuil C (2005) Ophiostomatoid and basidiomycetous fungi associated with green, red and grey lodgepole pines after mountain pine beetle (Dendroctonus ponderosae) infestation. Can J For Res 35: 274-284.
25. Kirisits T (2004) Fungal associates of European bark beetles with special emphasis on the 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.
26. Kirisits T (2010) Fungi isolated from Picea abies infested by the bark beetle Ips typographus in the Bialowieza forest in north-eastern Poland. For Pathol 40: 100-110.
27. Kirisits T, Offenthaler I (2002) Xylem sap flow of Norway spruce after inoculation with the blue-stain fungus Ceratocystis polonica. Plant Pathol 51: 359-364.
28. Kirisits T, Wingfield MJ, Chettri DB (2002) Studies on the association of blue-stain fungi with the Eastern Himalayan spruce bark beetle (Ips schmutzenhoferi) and with other bark beetles in Buthan. Yusipang Report, RNR RC Yusipang.
29. Kirschner R (2001) Diversity of filamentous fungi in bark beetle galleries in central Europe. In: Misra JK, Horn BW, Robert W (eds) Trichomycetes and other fungal groups. Science Publishers, Inc., pp 175-196.
30. Kirschner R, Oberwinkler F (1999) A new Ophiostoma species associated with bark beetles infesting Norway spruce. Can J Bot 77: 247-252.
31. Kirschner R, Begerow D, Oberwinkler F (2001a) A new Chionosphaera species associated with conifer inhabiting bark beetles. Mycol Res 105: 1403-1408.
32. Kirschner R, Sampaio JP, Gadanho M, Weiss M, Oberwinkler F (2001b) Cuniculitrema polymorpha (Tremellales, gen. nov. and sp. nov.), a heterobasidiomycete vectored by bark beetles, which is the teleomorph of Sterigmatosporidium polymorphum. Antoine van Leeuwenhoek 80: 149-161.
33. Klepzig KD, Raffa KF, Smalley EB (1991) Association of an insect-fungal complex with red pine decline in Wisconsin. Forest Sci 37: 1119-1139.
34. Kolařík M, Sláviková E, Pažoutová S (2006) The taxonomic and ecological characterization of the clinically important heterobasiodiomycete Fugomyces cyanescens and its association with bark beetles. Czech Mycol 58: 81-98.
35. Krokene P, Solheim H (1996) Fungal associates of five bark beetle species colonizing Norway spruce. Can J For Res 26: 2115-2122.
36. Lacap DC, Hyde KD, Liew ECY (2003) An evaluation of the fungal "morphotypes" concept based on ribosomial DNA sequences. Fungal Divers 12: 53-66.
37. Lee S, Kim JJ, Breuil C (2006) Diversity of fungi associated with mountain pine beetle, Dendroctonus ponderosae, and infested lodgepole pines in British Columbia. Fungal Divers 22: 91-105.
38. Leufvén A, Nehls L (1986) Quantification of different yeasts associated with the bark beetle, Ips typographus, during its attack on a spruce tree. Microb Ecol 12: 237-243.
39. Lieutier F, Yart A, Garcia J, Ham MC, Morelet M, Levieux J (1989) Champignons phytopathogènes associés à deux coléoptères scolytidae du pin sylvestres (Pinus sylvestris L.) et étude préliminaire de leur agressivité envers l'hôte. Ann For Sci 46: 201-216.
40. Lieutier F, Garcia J, Yart A, Vouland G, Pettinetti M, Morelet M (1991) Ophiostomatales (Ascomycètes) associées à Ips acuminatus Gyll (Coleoptera: Scolytitidae) sur le pin sylvestre (Pinus sylvestris L.) dans le Sud-Est de la France et comparison avec Ips sexdentatus Boern. Agronomie 11: 807-817.
41. Lim WY, 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: 79-94.
42. Linnakoski R, Wilhelm de Beer Z, Niemelä P, Wingfield MJ (2012) Associations of conifer-infesting bark beetles and fungi in Fennoscandia. Insects 3: 200-227.
43. Lumley TC, Gignac LD, Currah RS (2001) Microfungus communities of white spruce and trembling aspen logs at different stages of decay in disturbed and undisturbed sites in the boreal mixedwood region of Alberta. Can J Bot 79: 76-92.
44. Lygis V, Vasiliauskas R, Larsson KH, Stenlid J (2005) Wood-inhabiting fungi in stems of Fraxinus excelsior in declining ash stands of northern Lithuania, with particular reference to Armillaria cepistipes. Scand J For Res 20: 337-346.
45. Magurran A (2004) Measuring biological diversity. Blackwell Publishing, Oxford.
46. Mathiesen-Käärik A (1953) Eine Übersicht uber die gewöhnlichsten mit Borkenkäfern assoziierten Bläuepilze in Schweden einige für Sweden neue Bläuepilze. Med Stat Skogsf Inst Stockholm 43: 1-74.
47. Menkis A, Vasiliauskas R, Taylor AFS, Stenström 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.
48. Oberwinkler F, Kirschner R, Arenal F, Villarreal M, Rubio V, Begerow D, Bauer R (2006) Two new pycnidial members of the Atractiellales: Basidiopycnis hyaline and Proceropycnis pinicola. Mycologia 98: 637-649.
49. O'Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225-233.
50. Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42: 179-206.
51. PASW Statistics 18 (2009) Software version 18. 0. 0. SPSS Inc, Chicago.
52. Persson Y, Vasaitis R, Långström B, Öhrn 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 litter. Microb Ecol 58: 651-659.
53. Peverieri GS, Capretti P, Tiberi R (2006) Associations between Tomicus destruens and Leptographium spp. in Pinus pinea and Pinus pinaster stands in Tuscany, central Italy. For Pathol 36: 14-20.
54. Ragazzi A, Moricca S, Capretti P, Dellavalle I, Turco E (2003) Differences in composition of endophytic mycobiota in twigs and leaves of healthy and declining Quercus species in Italy. For Pathol 33: 31-38.
55. Rivera FN, Gómez Z, González E, López N, Hernández Rodríguez CH, Zúňiga G (2007) Yeasts associated with bark beetles of the genus Dendroctonus Erichson (Coleoptera, Curculionidae, Scolytinae): molecular identification and biochemical characterization. In: Bentz B, Cognato A, Raffa K (eds) Proceedings from the Third Workshop on genetics of bark beetles and associated microorganisms. Fort Collins, U. S., pp 45-48.
56. Roe AD, James PMA, Rice AV, Cooke JEK, Sperling FAH (2011) Spatial community structure of mountain pine beetle fungal symbionts across a latitudinal gradient. Microb Ecol 62: 347-360.
57. 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: 365-373.
58. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Springs Harbor Laboratory Press, New York.
59. Schweigkofler W, Otrosina WJ, Smith SL, Cluck DR, Maeda K, Peay KG, Garbelotto M (2005) Detection and quantification of Leptographium wageneri, the cause of black-stain root disease, from bark beetles (Coleoptera: Scolytidae) in Northern California using regular and real-time PCR. Can J For Res 35: 1798-1808.
60. Siemaszko W (1939) Zespoly grzbow towarzyszacych kornikom polskim. Planta Pol 7: 1-54.
61. Six DL, Bentz BJ (2003) Fungi associated with the North American spruce beetle, Dendroctonus rufipennis. Can J For Res 33: 1815-1820.
62. Smit E, Leeflang P, Glandorf B, van Elsas JD, Wernars K (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl Environ Microbiol 65: 2614-2621.
63. Solheim H (1986) Species of Ophiostomataceae isolated from Picea abies infested by the bark beetle Ips typographus. Nord J Bot 6: 199-207.
64. Solheim H (1992a) Fungal succession in sapwood of Norway spruce infested by the bark beetle Ips typographus. Eur J For Pathol 22: 136-148.
65. Solheim H (1992b) The early stages of fungal invasion in Norway spruce infested by the bark beetle Ips typographus. Can J Bot 70: 1-5.
66. Solheim H (1993a) Ecological aspects of fungi associated with the spruce bark beetle Ips typographus in Norway. In: Wingfield MJ, Seifert KA, Webber JF (eds) Ceratocystis and Ophiostoma. Taxonomy, ecology and pathogenicity. American Phytopathological Society, St. Paul, pp 235-242.
67. Solheim H (1993b) Fungi associated with the spruce bark beetle Ips typographus in an endemic area in Norway. Scand J For Res 8: 118-122.
68. Stergulc F, Frigimelica G, Faccoli M, Battisti A (2001) Pest and disease damage in natural and secondary conifer stands of the Friuli - Venezia Giulia (North-eastern Italy). In: Forster B, Knízek M, Grodzki W (eds) Methodology of forest insect and disease survey in central Europe. Proceeding of the IUFRO working party Busteni, Romania: Forest Research and Management Institute (ICAS), pp 167-169.
69. Vega EF, Dowd PF (2005) The role of yeast as insect endosymbionts. In: Vega FE, Blackwell M (eds) Insect-fungal associations: ecology and evolution. Oxford University Press, New York, pp 211-243.
70. Viiri H, Lieutier F (2004) Ophiostomatoid fungi associated with the spruce bark beetle, Ips typographus, in three areas in France. Ann Sci For 61: 215-219.
71. von Arx JA (1981) The genera of fungi sporulating in pure culture. J. Cramer, Vaduz.
72. Wang Y, Guo LD (2007) A comparative study of endophytic fungi in needles, bark, and xylem of Pinus tabulaeformis. Can J Bot 85: 911-917.
73. Wermelinger B (2004) Ecology and management of the spruce bark beetle Ips typographus - a review of recent research. For Ecol Manag 202: 67-82.
74. White TJ, Bruns TD, Lee S, Taylor JW (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 315-322.
75. Whitney HS (1982) Relationships between bark beetles and symbiotic organisms. In: Mitton JB, Sturgeon KB (eds) Bark beetles in North American Conifers: a system for study of evolutionary biology. University of Texas Press, Austin, pp 183-211.
76. Wichmann L, Ravn HP (2001) The spread of Ips typographus (L.) (Coleoptera, Scolytidae) attacks following heavy windthrow in Denmark, analysed using GIS. For Ecol Manag 148: 31-39.
77. Wingfield MJ, Seifert KA, Webber JF (1993) Ceratocystis and Ophiostoma. Taxonomy, ecology, and pathogenicity. American Phytopathological Society, St. Paul.
78. Yamaoka Y, Chung WH, Masuya H (2009) Constant association of ophiostomatoid fungi with the bark beetle Ips subelongatus invading Japanese larch logs. Mycoscience 50: 165-172.