Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers

Free Access

Review

Issue		Ann. For. Sci. Volume 66, Number 8, December 2009


Article Number		801
Number of page(s)		22
DOI		https://doi.org/10.1051/forest/2009066
Published online		25 November 2009

Anderbr, t O., Schlyter F. and Lofqvist J., 1988. Dynamics of tree attack in the bark beetle Ips typographus under semi-epidemic conditions. In: T.L. Payne and H. Saarenmaa (Eds.), Integrated control of Scolytid bark beetle, Blacksburg: Virginia Polytech Institute State University, pp. 35–51 [Google Scholar]
Aukema B.H., Werner R.A., Haberkern K.E., Illman B.L., Clayton M.K. and Raffa K.F., 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. Manage., 10, 187–202 [Google Scholar]
Ayres M.P., Wilkens R.T., Ruel J.J., Lombardero M.J. and Vallery E., 2000. Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi (Coleoptera: Scolytidae). Ecology 81: 2198–2210 [CrossRef] [Google Scholar]
Barras S.J., 1970. Antagonism between Dendroctonus frontalis and the fungus Ceratocystis minor. Ann. Entomol. Soc. Am. 63: 1187–1190 [Google Scholar]
Basham H.G., 1970. Wilt of loblolly pine inoculated with blue-stain fungi of the genus Ceratocystis. Phytopathology 60: 750–754 [CrossRef] [Google Scholar]
Ben Jamaa M.L., Lieutier F., Yart A., Jerraya A. and Khouja M.L., 2007. Phytopathogenic fungi associated with the bark beetles Tomicus piniperda and Orthotomicus erosus in Tunisia; study of the virulence of some isolates. For. Pathol. 37: 51–63. [CrossRef] [Google Scholar]
Berryman A.A., 1972. Resistance of conifers to invasion by bark beetle-fungus associations. BioScience 22: 298–602 [Google Scholar]
Berryman A.A., 1976. Theoretical explanation of mountain pine betle dynamics in lodgepole pine forests. Environ. Entomol. 5: 1225–1233 [Google Scholar]
Berryman A.A., 1982. Population dynamics of bark beetles. In: J.B. Mitton and K.B. Sturgeon (Eds.), Bark beetles in North American conifers, Austin, Univ. Texas, pp. 264–314 [Google Scholar]
Bleiker K.P. and Six D.L., 2007. Dietary benefits of fungal associates to an eruptive herbivore: potential implications of multiple associates on host population dynamics. Environ. Entomol. 36: 1384–1396 [CrossRef] [PubMed] [Google Scholar]
Bleiker K.P. and Six D.L., 2009. Competition and coexistence in a multi-partner mutualism: interactions between two fungal symbionts of the mountain pine beetle in beetle-attacked trees. Microb. Ecol. 57: 191–202 [CrossRef] [PubMed] [Google Scholar]
Bois E. and Lieutier F. 1997. Phenolic response of Scots pine clones to inoculation with Leptographium wingfieldii, a fungus associated with Tomicus piniperda. Plant Physiol.Biochem. 35: 819–825. [Google Scholar]
Bridges J.R., 1983. Mycangial fungi of Dendroctonus frontalis (Coleoptera: Scolytidae) and their relationship to beetle population trends. Environ. Entomol. 12: 858–861 [Google Scholar]
Bridges J.R., Nettleton W.A. and Conner M.D., 1985. Southern pine beetle (Coleoptera: Scolytidae) infestations without the blue-stain fungus, Ceratocystis minor. J. Econ. Entomol. 78: 325–27 [Google Scholar]
Brignolas F., Lieutier F., Sauvard D., Yart A., Drouet A. and Claudot A.-C., 1995. Changes in soluble phenol content of Norway spruce (Picea abies Karst.) phloem in response to wounding and inoculation with Ophiostoma polonicum. Eur. J. For. Pathol. 25: 253–65. [CrossRef] [Google Scholar]
Brignolas F., Lieutier F., Sauvard D., Christiansen E. and Berryman A.A., 1998. Phenolic predictors for Norway spruce resistance to the bark beetle Ips typographus (Coleoptera: Scolytidae) and an associated fungus, Ceratocystis polonica. Can. J. For. Res., 28: 720–28 [Google Scholar]
Cardoza Y.J., Klepzig K.D. and Raffa K.F., 2006. Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecol. Entomol. 31: 636–645 [CrossRef] [Google Scholar]
Cardoza Y.J., Moser J.C., Klepzig K.D. and Raffa K.F., 2008 Multipartite symbioses among fungi, mites, nematodes, and the spruce beetle, Dendroctonus rufipennis. Environ. Entomol. 37: 956–963. [CrossRef] [PubMed] [Google Scholar]
Chararas C., 1962. Scolytides des conifères. Lechevalier Ed., Paris, 556p [Google Scholar]
Christiansen E., 1985. Ceratocystis polonica inoculated in Norway spruce: Blue-staining in relation to inoculum density, resinosis and tree growth. Eur. J. For. Pathol. 15: 160–167 [CrossRef] [Google Scholar]
Christiansen E., 1985. Ips/Ceratocystis infection of Norway spruce: what is a deadly dosage? Z. Angew. Entomol. 99: 6–11 [CrossRef] [Google Scholar]
Christiansen E. and Glosli A.M., 1996. Mild drought enhances the resistance of Norway spruce to a bark beetle-transmitted blue-stain fungus. In: W.J. Mattson, P. Niemela and M. Rousi (Eds.), Dynamics of forest herbivory: Quest for pattern and principle, USDA For. Serv. Gen. Tech. Rep. NC-183, pp. 192–99 [Google Scholar]
Christiansen E., Waring R.H. and Berryman A.A., 1987. Resistance of conifers to bark beetle attacks: searching for general relationships. For. Ecol. Manage. 22: 89–106 [CrossRef] [Google Scholar]
Colineau B. and Lieutier F., 1994. Production of Ophiostoma-free adults of Ips sexdentatus Boern. (Coleoptera: Scolytidae) and comparison with naturally contaminated adults. Can. Entomol. 126: 103–10 [CrossRef] [Google Scholar]
Cook S.P. and Hain F.P., 1987. Four parameters of the wound response of loblolly and shortleaf pines to inoculations with the blue-staining fungus associated with the southern pine beetle. Can. J. Bot. 65: 2403–2409 [CrossRef] [Google Scholar]
Cook S.P., Hain F.P. and Nappen P.B., 1986. Seasonality of hypersensitive response by loblolly and shortleaf pine to inoculation with a fungal associate of the southern pine beetle (Coleoptera: Scolytidae). J. Entomol. Sci. 21: 283–285 [Google Scholar]
Coulson R.N., 1979, Poulation dynamics of bark beetles. Annu. Rev. Entomol. 24: 417–447. [CrossRef] [Google Scholar]
Croisé L. and Lieutier F., 1993, Effect of drought on the induced defence reaction of Scots pine to bark beetle associated fungi. Ann. Sci. for. 50: 91–97. [CrossRef] [Google Scholar]
Croisé L., Lieutier F. and Dreyer E., 1998. Scots pine responses to number and density of inoculation points with Leptographium wingfieldii Morelet, a bark beetle-associated fungus. Ann. Sci. For. 55: 497–506 [CrossRef] [Google Scholar]
Croisé L., Dreyer E. and Lieutier F., 1998b, Effects of drought stress and severe prunning on the reaction zone induced by single inoculations with a bark beetle associated fungus (Ophiostoma ips) in the phloem of young Scots pines. Can. J. For. Res. 28: 1814–1824. [CrossRef] [Google Scholar]
Delorme L. and Lieutier F., 1990. Monoterpene composition of the preformed and induced resins of Scots pine, and their effect on bark beetles and associated fungi. Eur. J. For. Pathol. 20: 304–16 [CrossRef] [Google Scholar]
Dymerski A.D., Anhold J.A. and Munson A.S., 2001. Spruce beetle (Dendroctonus rufipennis) outbreaks in Engelmann spruce (Picea engelmanni) in central Utah, 1986–1998. West. N. Am. Nat., 61: 19–24 [Google Scholar]
Eckhardt L.G., Goyer R.A., Klepzig K.D. and Jones J.P., 2004. Interactions of Hylastes species (Coleoptera: Scolytidae) with Leptographium species associated with loblolly pine decline. J. Econ. Entomol. 97: 468–474 [CrossRef] [PubMed] [Google Scholar]
Filip G.M., Christiansen E. and Parks C., 1989. Secondary resin production increases with vigor of Abies grandis inoculated with Trichosporium symbioticum in Northeastern Oregon. USDA FS PNW-RN 489, 1–10 [Google Scholar]
Franceschi V.R., Krokene P., Christiansen E. and Krekling T., 2005. Anatomical and chemical defenses of conifers against bark beetles and other pests. New Phytol. 167: 353–376 [CrossRef] [PubMed] [Google Scholar]
Francke-Grosmann H., 1963. Some new aspects in forest entomology. Annu. Rev. Entomol. 8: 415–438 [CrossRef] [Google Scholar]
Francke-Grosmann H., 1967. Ectosymbiosis in wood-inhabiting insects. In: S.M. Henry (Ed.), Symbiosis, Vol. 2, Academic Press, New York, London. [Google Scholar]
Furniss R.L. and Carolin V.M., 1977. Western Forest Insects. USDA For. Serv. Misc. Publ. N°1339, 1339, 654 p [Google Scholar]
Grégoire J.C. and Evans H.F., 2004. Damage and control of BAWBILT organisms, an overview. In: F. Lieutier, K.R. Day, A. Battisti, J.C. Grégoire and H.J. Evans (Eds.), Bark and wood boring insects in living trees in Europe, a synthesis, Kluwer Acad. Publ., Dordrecht, pp. 19–37. [Google Scholar]
Guérard N., Dreyer E. and Lieutier F., 2000. Interactions between Scots pine, Ips acuminatus (Gyll.) and Ophiostoma brunneo-ciliatum (Math.): estimation of critical thresholds of attack and inoculation densities and effect on hydraulic properties of the stem. Ann. For. Sci. 57: 681–690 [CrossRef] [EDP Sciences] [Google Scholar]
Harding S., 1989. The influence of mutualistic blue-stain fungi on bark beetle population dynamics. Ph.D thesis, Royal Veterinary and Agricultural University Copenhagen. [Google Scholar]
Harrington T.C., 1993. Diseases of conifers caused by species of Ophiostoma and Leptographium. In: M.J. Wingfield, K.A. Seifert and J.F. Webber (Eds.), Ophiostoma and Ceratocystis: Taxonomy, Ecology and Pathogenicity, APS Press, St Paul, Minnesota, pp. 161–172. [Google Scholar]
Harrington T.C., 1993. Biology and taxonomy of fungi associated with bark beetles. In: T.D. Schowalter and G.M. Filip (Eds.), Beetle-Pathogen Interactions in Conifer Forests, New York: Academic Press, pp. 37–58. [Google Scholar]
Harrington T.C., 2005. Ecology and evolution of mycetophagous bark beetles and their fungal partners. In: F.E. Vega and M. Blackwell (Eds.), Insect-fungal associations, ecology and evolution, Oxford University Press, pp. 257–289. [Google Scholar]
Harrington T.C. and Cobb F.W. Jr., 1983. Pathogenicity of Leptographium and Verticicladiella spp. Isolated from roots of western North American conifers. Phytopathology 73: 596–599. [CrossRef] [Google Scholar]
Harrington T.C. and Wingfield M.J., 1998. The Ceratocystis species on conifers. Can. J. Bot. 76: 1446–57 [CrossRef] [Google Scholar]
Hetrick L.A., 1949. Some overlooked relationships of southern pine beetle. J. Econ. Entomol. 42: 466–469 [Google Scholar]
Highley L. and Tattar T.A., 1985. Leptographium terebrantis and black turpentine beetles associated with blue stain and mortality of black and Scots pine on Cape Cod, Massachussets. Plant Dis. 69: 528–530 [CrossRef] [Google Scholar]
Hobson K.R., Parmeter J.R. Jr. and Wood D.L. 1994. The role of fungi vectored by Dendroctonus brevicomis Leconte (Coleoptera: Scolytidae) in occlusion of ponderosa pine xylem. Can. Entomol. 126: 277–282. [CrossRef] [Google Scholar]
Hofstetter R.W., Cronin J.T., Klepzig K.D., Moser J.C. and Ayres M.P., 2006. Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle. Oecologia, 147: 679–691. [CrossRef] [PubMed] [Google Scholar]
Hofstetter R.W., Dempsey T.D., Klepzig K.D. and Ayres M.P., 2007. Temperature-dependent effects on mutualistic, antagonistic, and commensalistic interactions among insects, fungi and mites. Community Ecol. 8: 47–56 [CrossRef] [Google Scholar]
Horntvedt R., Christiansen E., Solheim H., Wang and S., 1983. Artificial inoculation with Ips typographus-associated blue-stain fungi can kill healthy Norway spruce trees. Medd. fra Norsk. Skogforsk. 38: 1–20 [Google Scholar]
Jacobs K. and Wingfield M.J., 2001. Leptographium species, Insect associates and Agents of Blue Stain, APS Press, St Paul, Minnesota, 207 p [Google Scholar]
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 [CrossRef] [Google Scholar]
Kelley S.T. and Farrell B.D., 1998. Is specialization a dead end? The phylogeny and host use in Dendroctonus bark beetles (Scolytidae). Evolution 52: 1731–1743 [CrossRef] [PubMed] [Google Scholar]
Kim J-J., Plattner A., Lim Y.W. and Breuil C., 2008. Comparison of two methods to asses the virulence of the mountain pine beetle associate, Grosmannia clavigera, to Pinus contorta. Scand. J. For. Res. 23: 98–104 [CrossRef] [Google Scholar]
Kirisits T., 1998. Pathogenicity of three blue-stain fungi associated with the bark beetle Ips typographus to Norway spruce in Austria. Österr. Z. Pilzk. 7: 191–201 [Google Scholar]
Kirisits T., 1999. Report on a strain of the pathogenic blue-stain fungus Ceratocystis polonica with low virulence. Osterr. Z. Piltz. 8: 157–167 [Google Scholar]
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 thesis, Universitat fur Bodenkultur Wien. [Google Scholar]
Kirisits T., 2004. Fungal associates of European bark beetles with special emphasis on the Ophiostomatoid fungi. In: F. Lieutier, K.R. Day, A. Battisti, J.C. Grégoire and H.F. Evans (Eds.), Bark and wood boring insects in living trees in Europe, a synthesis, Kluwer, Dordrecht, pp. 181–235. [CrossRef] [Google Scholar]
Kirisits T., Grubelnik R. and Führer E., 2000. Die ökologische Bedeutung von Bläuepilzen für rindenbrütende Borkenkäfer. In: F. Müller (Ed.), Mariabrunner Waldbautage 1999 – Umbau sekundärer Nadelwälder, Vienna, Schriftenreihe der Forstlichen Bundesversuchsanstalt Wien, FBVA-Berichte, 111, pp. 117--137. [Google Scholar]
Klepzig K.D. and Six D.L., 2004. Bark beetle-fungal symbiosis: context dependency in complex associations. Symbiosis 37: 189–205 [Google Scholar]
Klepzig K.D., Raffa K.F. and Smalley E.B., 1991. Association of an insect-fungal complex with red pine decline in Wisconsin. For. Sci. 37: 1119–1139 [Google Scholar]
Klepzig K.D., Smalley E.B. and Raffa K.F., 1995. Dendroctonus valens and Hylastes porculus (Coleoptera: Scolytidae): vectors of pathogenic fungi (Ophiostomatales) associated with red pine decline disease. Great Lakes Entomol. 28: 81–87 [Google Scholar]
Klepzig K.D., Moser J.C., Lombardero M.J., Ayres M.P., Hofstetter R.W. and Walkinshaw C.J., 2001. Mutualism and antagonism: ecological interactions among bark beetles, mites and fungi. In: M.J. Jeger and N.J. Spence (Eds.), Biotic interactions in plant-pathogen associations, CAB International, pp. 237–267. [CrossRef] [Google Scholar]
Klepzig K.D., Moser J.C., Lombardero F.J., Hofstetter R.W. and Ayres M.P., 2001. Symbiosis and competition: complex interactions among beetles, fungi and mites. Symbiosis 30: 83–96 [Google Scholar]
Knizek M. and Beaver R., 2004. Taxonomy and systematic of bark and ambrosia beetles. In: F. Lieutier, K.R. Day, A. Battisti, J.C. Grégoire and H.J. Evans (Eds.), Bark and wood boring insects in living trees in Europe, a synthesis, Kluwer Acad. Publ., Dordrecht, pp. 41–54. [CrossRef] [Google Scholar]
Krokene P. 1996. The role of blue-stain fungi in tree-killing by bark beetles. Thesis, University of Oslo. [Google Scholar]
Krokene P. and Solheim H., 1997. Growth of four bark-beetle-associated blue-stain fungi in relation to the induced wound response in Norway spruce. Can. J. Bot. 75: 618–625 [CrossRef] [Google Scholar]
Krokene P. and Solheim H., 1998. Pathogenicity of four blue-stain fungi associated with aggressive and nonaggressive bark beetles. Phytopathology 88: 39–44 [CrossRef] [PubMed] [Google Scholar]
Krokene P. and Solheim H., 1999. What do low density inoculations with fungus tell us about fungal virulence and tree resistance? In: Lieutier F. Mattson W.J. and Wagner M.R. (Eds.), Physiology and genetics of tree-phytophage interactions, INRA Editions, Versailles, pp. 353–362. [Google Scholar]
Långström B. and Hellqvist C., 1988. Scots pine resistance against Tomicus piniperda as related to tree vitality and attack density. In: Payne T.L. and Saarenmaa H. (Eds.), Integrated control of scolytid bark beetles, ginia Polytech. Inst. St. Univ.Blacksburg, pp. 121–133. [Google Scholar]
Långström B. and Hellqvist C., 1993. Scots pine susceptibility to attack by Tomicus piniperda (L) as related to pruning date and attack density. Ann. Sci. For. 50: 101–117 [Google Scholar]
Långström B., Hellqvist C., Ericsson A. and Gref D., 1992. Induced defense reaction in Scots pine following stem attacks by Tomicus piniperda L. Ecography 15: 318–327 [CrossRef] [Google Scholar]
Långström B., Solheim H., Hellqvist C. and 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. For. Pathol. 23: 400–415 [CrossRef] [Google Scholar]
Lee S., Kim J.-J. and Breuil C., 2006. Diversity of fungi associated with mountain pine beetle, Dendroctonus ponderosae, and infested lodgepole pines in British Columbia. Mountain Pine beetle Research Initiative Working Paper 2006-06, 20 p [Google Scholar]
Lévieux J., Cassier P., Guillaumin D. and Roques A., 1991. Structures implicated in the transportation of pathogenic fungi by the European bark beetle, Ips sexdentatus Boerner: Ultrastructure of a mycangium. Can. Entomol. 123: 245–54 [CrossRef] [Google Scholar]
Lieutier F., 1992. Les réactions de défense des conifères et stratégies d’attaque de quelques Scolytides européens. Mém. Soc. Roy. belge Entomol. 35: 529–539 [Google Scholar]
Lieutier F., 1995. Associated fungi, induced reaction and attack strategy of Tomicus piniperda (Coleoptera: Scolytidae) in Scots pine. In: F.P. Hain, S.M. Salom, W.F. Ravlin, T.L. Payne and K.F. Raffa (Eds.), Behavior, Population Dynamics and Control of Forest Insects, Proceedings International Union Forestry Research Organizations Joint Conference, February 1994 Maui, Hawai, pp. 139–153. [Google Scholar]
Lieutier F., 2002. Mechanisms of resistance in conifers and bark beetle attack strategies. In: M.R. Wagner, K.M. Clancy, F. Lieutier and T.D. Paine (Eds.), Mechanisms and deployment of resistance in trees to insects, Kluwer, Dordrecht, pp. 31–75. [CrossRef] [Google Scholar]
Lieutier F., 2004. Host resistance to bark beetles and its variations. In: F. Lieutier, K.Day, A. Battisti, J.C. Grégoire and H. Evans (Eds.), Bark and wood boring insects in living trees in Europe, A synthesis, Kluwer, Dordrecht, pp. 135–180. [CrossRef] [Google Scholar]
Lieutier F., Yart A., Garcia J., Poupinel B. and Lévieux J., 1988. Do fungi influence the establishment of bark beetles in Scots pine? In: W.J. Mattson, J. Lévieux and C. Bernard-Dagan (Eds.), Mechanisms of woody plant defenses against insects: search for pattern, Springer, New York, pp. 321–334. [Google Scholar]
Lieutier F., Cheniclet C. and Garcia J., 1989. Comparison of the defense reactions of Pinus pinaster and Pinus sylvestris to attacks by two bark beetles (Coleoptera: Scolytidae) and their associated fungi. Environ. Entomol. 18: 228–234 [Google Scholar]
Lieutier F., Yart A., Garcia J., Ham M.C., Morelet M. and Lévieux 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. Sci. For. 46: 201–216 [CrossRef] [Google Scholar]
Lieutier F., Yart A., Garcia J. and Ham M-C., 1990. Cinétique de croissance des champignons associés à Ips sexdentatus Boern. et à Tomicus piniperda L. (Coleoptera: Scolytidae) et des réactions dedéfense des pins sylvestres (Pinus sylvestris L.) inoculés. Agronomie 10: 243–56. [CrossRef] [Google Scholar]
Lieutier F., Yart A., Jay-Allemand C. and Delorme L. 1991a. Preliminary investigations on phenolics as a response of Scots pine phloem to attacks by bark beetles and associated fungi. Eur. J. For. Pathol. 21: 354–354. [CrossRef] [Google Scholar]
Lieutier F., Garcia J., Yart A., Voul, G., Pettinetti M. and Morelet M., 1991. Ophiostomatales (Ascomycetes) associées à Ips acuminatus (Coleoptera: Scolytidae) sur le pin sylvestre (Pinus sylvestris) dans le Sud-Est de la France, et comparaison avec Ips sexdentatus Boern. Agronomie 11: 807–817 [CrossRef] [Google Scholar]
Lieutier F., Voul, G., Pettinetti M., Garcia J., Romary P. and Yart A., 1992. Defence reactions of Norway spruce (Picea abies Karst.) to artificial insertion of Dendroctonus micans Kug. (Coleoptera: Scolytidae). J. Appl. Entomol. 114: 174–186 [CrossRef] [Google Scholar]
Lieutier F., Garcia J., Yart A. and Romary P., 1995. Wound reaction of Scots pine (Pinus sylvestris L.) to attacks by Tomicus piniperda L. and Ips sexdentatus Boern. (Coleoptera: Scolytidae). J. Appl. Entomol. 119: 591–600 [CrossRef] [Google Scholar]
Lieutier F., Sauvard D., Brignolas F., Picron V., Yart A., Bastien C., Jay-Allem and C., 1996. Changes in phenolic metabolites of Scots pine phloem induced by Ophiostoma brunneo-ciliatum, a bark-beetle-associated fungus. Eur. J. For. Pathol., 26, 145–158 [Google Scholar]
Lieutier F., Yart A., Ye H., Sauvard D. and Gallois V., 2004. Between-isolate variations in the performances of Leptographium wingfieldii Morelet, a fungus associated with the bark beetle Tomicus piniperda L. Ann. For. Sci. 61: 45–53 [CrossRef] [EDP Sciences] [Google Scholar]
Lieutier F., Ghaioule D. and Yart A., 2005. Virulence and possible role of fungi associated with the bark beetles Tomicus piniperda L., and Orthotomicus erosus Woll. in Morocco. In: F. Lieutier and D. Ghaioule (Eds.), Entomological research in Mediterranean ecosystems, INRA Ed., Versailles, pp. 195–208. [Google Scholar]
Mathiesen A., 1950. Über einige mit Borkenkäfern assoziierte Bläuepilze in Schweden. Oikos 2: 275–308 [CrossRef] [Google Scholar]
Mathiesen-Käärik A., 1953. Eine Übersicht über die gewöhnlichsten mit Borkenkäfern assoziierten Bläuepilze in Schweden und einige für Schweden neue Bläuepilze. Meddel. Frå. Stat. Skogforsk. Inst. 43: 1–74 [Google Scholar]
Mathre D.E., 1964. Survey of Ceratocystis spp. associated with bark beetles in California. Contrib. Boyce Thomp. Inst. 22: 353–361 [Google Scholar]
Mathre D.E., 1964. Pathogenicity of Ceratocystis ips and Ceratocystis minor to Pinus ponderosa. Contrib. Boyce Thomp. Inst. 22: 363–388 [Google Scholar]
Neal T.A. and Ross D.W., 1999. Pathogenicity to western larch (Larix occidentalis) of two fungi, Ophiostoma pseudotsugae and Leptographium abietinum, associated with the Douglas fir beetle (Coleoptera: Scolytidae). Agric. For. Entomol. 1: 203–207 [CrossRef] [Google Scholar]
Nebeker T.E., Hodges J.D. and Blanche C.A. 1993. Host Response to Bark Beetle and Pathogen Colonization. In. T.D. Schowalter and G.M. Filip (Eds.), Beetle Pathogen Interactions in Conifer Forests, Academic Press, San Diego, pp. 157–173. [Google Scholar]
Owen D.R., Lindahl K.Q., Wood D.L. and Parmeter J.R.Jr., 1987. Pathogenicity of fungi isolated from Dendroctonus valens, D. brevicomis and D. ponderosae to ponderosa pine seedlings. Phytopathology 77: 631–636. [Google Scholar]
Paine T.D. and Birch M.C., 1983. Acquisition and maintenance of mycangial fungi by Dendroctonus brevicomis LeConte (Coleoptera: Scolytidae). Environ. Entomol. 12: 1384–1386 [Google Scholar]
Paine T.D. and Stephen F.M., 1987. Fungi associated with the southern pine beetle: avoidance of induced defense response in loblolly pine. Oecologia 74: 377–379 [CrossRef] [PubMed] [Google Scholar]
Paine T.D., Raffa K.F. and Harrington T.C., 1997. Interactions among Scolytid bark beetles, their associated fungi, and live host conifers. Annu. Rev. Entomol. 42: 179–206 [CrossRef] [PubMed] [Google Scholar]
Parmeter J.R., Slaughter G.W., Chen M.M. and Wood D.L., 1992. Rate and depth of sapwood occlusion following inoculation of ponderosa pine with bluestain fungi. For. Sci. 38: 34–44 [Google Scholar]
Payne T.L., 1980. Life History & Habits. In: R.C. Thatcher, J.L. Searcy, J.E. Coster and G.D. Hertel (Eds.), The southern pine beetle, USDA For. Serv. Sci. Educ. Admin. Tech. Bull. N° 1631, pp. 7–28. [Google Scholar]
Plattner A., Kim J-J., DiGiustini S. and Breuil C., 2008. Variation in pathogenicity of a mountain pine beetle-associated fungus, Grosmannia clavigera, on young lodgepole pine in British Columbia. Can J. Plant Pathol. 30: 1–10 [CrossRef] [Google Scholar]
Raffa K.F., 1991. Induced defensive reactions in conifer-bark beetle systems. In: D.W. Tallamy and M.J. Raupp (Eds.), Phytochemical induction by herbivore, Wiley and Sons, pp. 245–276. [Google Scholar]
Raffa K.F., 2001. Mixed messages across multiple trophic levels: the ecology of bark beetle chemical communication systems. Chemoecology 11: 49-65 [CrossRef] [Google Scholar]
Raffa K.F. and Berryman A.A., 1982. Accumulation of monoterpenes and associated volatiles following fungal inoculation of grant fir with a fungus transmitted by the fir engraver Scolytus ventralis (Coleoptera: Scolytidae). Can. Entomol. 114: 797-810 [CrossRef] [Google Scholar]
Raffa K.F. and Berryman A.A., 1982. Gustatory cues in the orientation of Dendroctonus ponderosae (Coleoptera: Scolytidae) to host trees. Can. Entomol. 114: 97-104 [CrossRef] [Google Scholar]
Raffa K.F. and Berryman A.A., 1983. The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). Ecol. Monog. 53: 27–49 [CrossRef] [Google Scholar]
Raffa K.F. and Berryman A.A., 1983. Physiological aspects of lodgepole pine wound responses to a fungal symbiont of the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae). Can. Entomol. 115: 723–34 [CrossRef] [Google Scholar]
Raffa K.F. and Klepzig K.D., 1992. Tree defense mechanisms against fungi associated with insects. In: R.A. Blanchette and A.R. Biggs (Eds.), Defense Mechanisms of Woody Plants Against Fungi, Springer, New York, pp. 354–389. [Google Scholar]
Raffa K.F. and Smalley E.B., 1988. Response of red and Jack pines to inoculation with microbial associates of the pine engraver,Ips pini (Coleoptera: Scolytidae). Can. J. For. Res. 18: 581–586 [CrossRef] [Google Scholar]
Raffa K.F., Phillips T.W. and Salom S.M., 1993. Strategies and mechanisms of host colonization by bark beetles. In: Schowalter T.D. and Filip G.M. (Eds.), Beetle-pathogen interactions in conifer forests, Academic Press, San Diego, pp. 103–128. [Google Scholar]
Rane K.K. and Tattar T.A., 1987. Pathogenicity of blue stain fungi associated with Dendroctonus terebrans. Plant Dis. 71: 879–883 [CrossRef] [Google Scholar]
Redfern D.B., Stoakley J.T., Steele H. and Minter D.W., 1987. Dieback and death of larch caused by Ceratocystis laricicola sp. nov. following attack by Ips cembrae. Plant Pathol. 36: 467–80 [CrossRef] [Google Scholar]
Reid R.W., Whitney H.S. and Watson J.A., 1967. Reactions of lodgepole pine to attack by Dendroctonus ponderosae Hopkins and blue stain fungi. Can. J. Bot. 45: 115–126 [Google Scholar]
Rennerfelt E., 1950. Über den Zusammenhang zwischen dem Verblauen des Holzes und den Insekten. Oikos 2: 120–37 [CrossRef] [Google Scholar]
Reynolds K.M., 1992. Relations between activity of Dendroctonus rufipennis Kirby on Lutz spruce and blue stain associate with Leptographium abietinum (Peck) Wingfield. For. Ecol. Manage. 47: 71–86 [CrossRef] [Google Scholar]
Rice A.V., Thormann M.N. and Langor D.W., 2007. Mountain pine beetle associated blue-stain fungi cause lesions on jack pine, lodgepole pine, and lodgepole x jack pine hybrids in Alberta. Can. J. Bot. 85: 307–315 [CrossRef] [Google Scholar]
Rice A.V., Thormann M.N. and Langor D.W., 2007. Virulence of, and interactions among, mountain pine beetle associated blue-stain fungi on two pine species and their hybrids in Alberta. Can. J. Bot. 85: 316–323 [CrossRef] [Google Scholar]
Rice A.V., Thormann M.N. and Langor D.W., 2008. Mountain pine beetle-associated blue-stain fungi are differentially adapted to boreal temperatures. For. Pathol. 38: 113–123 [CrossRef] [Google Scholar]
Ross D.W. and Solheim H., 1997. Pathogenicity to Douglas fir of Ophiostoma pseudotsugae and Leptographium abietinum, fungi associated with the Douglas fir beetle. Can. J. For. Res. 27: 39–43 [CrossRef] [Google Scholar]
Ross D.W., Fenn P. and Stephen F.M., 1992. Growth of southern pine beetle associated fungi in relation to the induced wound response in loblolly pine. Can. J. for. Res. 22: 1851–1859 [CrossRef] [Google Scholar]
Russel C.E. and Berryman A.A., 1976. Host resistance to the fir engraver. 1. Monoterpene composition of Abies grandis pitch blisters and fungus-infested wounds. Can. J. Bot. 54: 14–18 [CrossRef] [Google Scholar]
Safranyik L., Shrimpton D.M. and Whitney H.S., 1975. An Interpretation of the Interaction Between Lodgepole Pine, the Mounain Pine Beetle and its Associated Blue Stain Fungi in Western Canada. In: D. Baumgartner (Ed.), Management of Lodgepole Pine Ecosystems, Pullman: Wash. State Univ. Coop. Ext. Serv., pp. 406–428. [Google Scholar]
Sallé A., Monclus R., Yart A., Garcia J., Romary P. and 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 [CrossRef] [Google Scholar]
Sallé A., Ye H., Yart A. and Lieutier F., 2008. Pinus yunnanensis resistance to a bark beetle associated fungus is increased during a natural water stress. Tree Physiol. 28: 679–687 [PubMed] [Google Scholar]
Siemaszko W., 1939. Zepoly grzybów towarzyszacych kornikom polskim [Fungi associated with bark-beetles in Poland]. Planta Polonica 7: 1–54 [Google Scholar]
Six D.L., 2003. Bark beetle-fungus symbiosis. In: T. Miller and K. Kourtzis (Eds.), Insect symbiosis, CRC Press, pp. 97–114. [CrossRef] [Google Scholar]
Six D.L. and Bentz B.J., 2003. Fungi associated with the North American spruce beetle, Dendroctonus rufipennis. Can. J. For. Res. 33: 1815–1820 [CrossRef] [Google Scholar]
Six D.L. and Bentz B.J., 2007. Temperature determines symbiont abundance in a multipartite bark beetle-fungus ectosymbiosis. Microb. Ecol. 54: 112–118 [CrossRef] [PubMed] [Google Scholar]
Six D.L. and Klepzig K.D., 2004. Dendroctonus bark beetles as model systems for studies on symbiosis. Symbiosis 37: 207–232 [Google Scholar]
Six D.L. and Paine T.D., 1997. Ophiostoma clavigerum is the mycangial fungus of the Jeffrey pine beetle, Dendroctonus jeffreyi. Mycologia 89: 858–866 [CrossRef] [Google Scholar]
Six D.L. and Paine T.D., 1998. Effects of mycangial fungi and host tree species on progeny survival and emergence of Dendroctonus ponderosae (Coleoptera: Scolytidae). Environ. Entomol. 27: 1393–1401 [Google Scholar]
Six D.L. and Paine T.D., 1999. Phylogenetic comparison of ascomycete mycangial fungi and Dendroctonus bark beetles (Coleoptera: Scolytidae). Ann. Entomol. Soc. Am. 91: 159–166 [Google Scholar]
Solheim H., 1986. Species of Ophiostomataceae isolated from Picea abies infested by the bark beetle Ips typographus. Nord. J. Bot. 6: 199–207 [CrossRef] [Google Scholar]
Solheim H., 1988. Pathogenicity of some Ips typographus associated blue-stain fungi to Norway spruce. Medd. fra Norsk. Inst. Skogforsk. 40: 1–11 [Google Scholar]
Solheim H., 1991. Oxygen deficiency and spruce resin inhibition of growth of fungi associated with Ips typographus. Mycol. Res. 95: 1387–1392 [CrossRef] [Google Scholar]
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 [CrossRef] [Google Scholar]
Solheim H., 1992. Fungal succession in sapwood of Norway spruce infested by the bark beetle Ips typographus. Eur. J. For. Pathol. 22: 136–48 [CrossRef] [Google Scholar]
Solheim H., 1993. Ecological aspects of fungi associated with the spruce bark beetle Ips typographus in Norway. In: Wingfield M.J., Seifert K.A. and Webber J.F. (Eds.), Ceratocystis and Ophiostoma: taxonomy, ecology and pathogenicity, APS Press, St Paul, Minnesota, pp. 235--242. [Google Scholar]
Solheim H., 1993. Fungi associated with the spruce bark beetle Ips typographus in an endemic area in Norway. Scand. J. For. Res. 8: 118–122 [CrossRef] [Google Scholar]
Solheim H. and 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 [CrossRef] [Google Scholar]
Solheim H. and Krokene P., 1998. Growth and virulence of Ceratocystis rufipenni and three blue-stain fungi isolated from the Douglas-fir beetle. Can. J. Bot. 76: 1763–1769 [CrossRef] [Google Scholar]
Solheim H. and Långström B., 1991. Blue stain fungi associated with Tomicus piniperda in Sweden and preliminary observation on their pathogenicity. Ann. Sci. For. 48: 149–156 [CrossRef] [Google Scholar]
Solheim H. and Safranyik L., 1997. Pathogenicity to Sitka spruce of Ceratocystis rufipenni and Leptographium abietinum, blue-stain fungi associated with the spruce bark beetle. Can. J. For. Res. 27: 1336–1341 [CrossRef] [Google Scholar]
Solheim H., Långström B. and 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. For. Res. 23: 1438–1443 [CrossRef] [Google Scholar]
Solheim H., Krokene P. and 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: 111–16 [CrossRef] [Google Scholar]
Stephen F.M., Berisford C.W., Dahlsten D.L., Fenn P. and Moser J.C., 1993. Invertebrate and microbial associates. In: Schowalter T. and Filip G. (Eds.), Beetle-pathogen interactions in conifer forests, Academic, San Diego, pp. 129–153. [Google Scholar]
Uzunovic A. and Webber J.F., 1998. Comparison of blue stain fungi grown in vitro and in freshly cut pine billets. Eur. J. For. Pathol. 28: 323–334 [CrossRef] [Google Scholar]
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: 529–33 [CrossRef] [Google Scholar]
Viiri H. and Lieutier F., 2004. Ophiostomatoid fungi associated with the spruce bark beetle, Ips typographus, in post-epidemic areas in France. Ann. For. Sci. 61: 215–219 [CrossRef] [EDP Sciences] [Google Scholar]
Wallin K.F. and Raffa K.H., 2001. Effects of folivory on subcortical plant defenses: can defense theories predict interguild processes? Ecology 82: 1387–1400 [CrossRef] [Google Scholar]
Waring R.H. and Pitman G.B., 1983. Physiological stress in lodgepole pine as a precursor for mountain pine beetle attack. Z. Angew. Entomol. 96: 265–270 [CrossRef] [Google Scholar]
Whitney H.S., 1982. Relationships between bark beetles and symbiotic organisms. In: Mitton J.B. and Sturgeon K.B. (Eds.), Bark beetles in North American conifers, Austin, Univ. Texas Press, pp. 183–211. [Google Scholar]
Whitney H.S. and Cobb F.W., 1972. Non-staining fungi associated with the bark beetle Dendroctonus brevicomis (Coleoptera: Scolytidae) on Pinus ponderosa. Can. J. Bot. 50: 1943–1945 [CrossRef] [Google Scholar]
Whitney H.S. and Farris S.H., 1970. Maxillary mycangium in the mountain pine beetle. Science 167: 54–55 [CrossRef] [PubMed] [Google Scholar]
Wingfield M.J., 1983. Association of Verticicladiella procera and Leptographium terebrantis with insects in the lake states. Can. J. For. Res. 13: 1238–1245 [CrossRef] [Google Scholar]
Wingfield M.J., Seifert K.A. and Webber J.F., 1993. Ceratocystis and Ophiostoma: taxonomy, ecology, and pathogenicity, APS Press, 293 p [Google Scholar]
Wong B.E. and Berryman A.A., 1977. Host resistance to the fir engraver beetle. 3. Lesion development and containment of infection by resistant Abies grandis inoculated with Trichosporium symbioticum. Can. J. Bot. 55: 2358–2365 [CrossRef] [Google Scholar]
Wood D.L., 1982. The role of pheromones, kairomones, and allomones in the host selection and behavior of bark beetles. Annu. Rev. Entomol. 27: 411–446 [CrossRef] [Google Scholar]
Wullschleger S.D., McLaughlin S.B. and Ayres M.P., 2004. High resolution analysis of stem increment and sap flow for loblolly pine trees attacked by southern pine beetle. Can. J. For. Res. 34: 2387–2393 [CrossRef] [Google Scholar]
Yamaoka Y., Hiratsuka Y. and Maruyama P.J., 1995. The ability of Ophiostoma clavigerum to kill mature lodgepole pine trees. Eur. J. For. Pathol. 25: 401–404 [CrossRef] [Google Scholar]