Interactions among Norway spruce, the bark beetle Ips typographus and its fungal symbionts in times of drought
Status PubMed-not-MEDLINE Language English Country Germany Media print-electronic
Document type Journal Article, Review
Grant support
V 631
Austrian Science Fund FWF - Austria
PubMed
34720785
PubMed Central
PMC8550215
DOI
10.1007/s10340-021-01341-y
PII: 1341
Knihovny.cz E-resources
- Keywords
- Drought, Ophiostomatoid fungi, Picea abies, Specialised metabolites, Spruce bark beetle, Tree defence,
- Publication type
- Journal Article MeSH
- Review MeSH
Resilience and functionality of European Norway spruce forests are increasingly threatened by mass outbreaks of the bark beetle Ips typographus promoted by heat, wind throw and drought. Here, we review current knowledge on Norway spruce and I. typographus interactions from the perspective of drought-stressed trees, host selection, colonisation behaviour of beetles, with multi-level effects of symbiotic ophiostomatoid fungi. By including chemo-ecological, molecular and behavioural perspectives, we provide a comprehensive picture on this complex, multitrophic system in the light of climate change. Trees invest carbon into specialised metabolism to produce defence compounds against biotic invaders; processes that are strongly affected by physiological stress such as drought. Spruce bark contains numerous terpenoid and phenolic substances, which are important for bark beetle aggregation and attack success. Abiotic stressors such as increased temperatures and drought affect composition, amounts and emission rates of volatile compounds. Thus, drought events may influence olfactory responses of I. typographus, and further the pheromone communication enabling mass attack. In addition, I. typographus is associated with numerous ophiostomatoid fungal symbionts with multiple effects on beetle life history. Symbiotic fungi degrade spruce toxins, help to exhaust tree defences, produce beetle semiochemicals, and possibly provide nutrition. As the various fungal associates have different temperature optima, they can influence the performance of I. typographus differently under changing environmental conditions. Finally, we discuss why effects of drought on tree-killing by bark beetles are still poorly understood and provide an outlook on future research on this eruptive species using both, field and laboratory experiments.
See more in PubMed
Adams HD, Germino MJ, Breshears DD, Barron-Gafford GA, Guardiola-Claramonte M, Zou CB, Huxman TE. Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism. New Phytol. 2013;197:1142–1151. doi: 10.1111/nph.12102. PubMed DOI
Allen CD, Macalady AK, Chenchouni H, et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag. 2010;259:660–684. doi: 10.1016/j.foreco.2009.09.001. DOI
Andersson MN. Mechanisms of odor coding in coniferous bark beetles: From neuron to behavior and application. Psyche (Camb Mass) 2012;2012:1–14. doi: 10.1155/2012/149572. DOI
Andersson MN, Larsson MC, Schlyter F. Specificity and redundancy in the olfactory system of the bark beetle Ips typographus: single-cell responses to ecologically relevant odors. J Insect Physiol. 2009;55:556–567. doi: 10.1016/j.jinsphys.2009.01.018. PubMed DOI
Andersson MN, Larsson MC, Blazenec M, Jakuš R, Zhang QH, Schlyter F. Peripheral modulation of pheromone response by inhibitory host compound in a beetle. J Exp Biol. 2010;213:3332–3339. doi: 10.1242/jeb.044396. PubMed DOI
Andersson MN, Grosse-Wilde E, Keeling C, et al. Antennal transcriptome analysis of the chemosensory gene families in the tree killing bark beetles, Ips typographus and Dendroctonus ponderosae (Coleoptera: Curculionidae: Scolytinae) BMC Genom. 2013;14:198. doi: 10.1186/1471-2164-14-198. PubMed DOI PMC
Andersson MN, Löfstedt C, Newcomb RD. Insect olfaction and the evolution of receptor tuning. Front Ecol Evol. 2015 doi: 10.3389/fevo.2015.00053. DOI
Arango-Velez A, Gonzalez LM, Meents MJ, et al. Influence of water deficit on the molecular responses of Pinus contorta x Pinus banksiana mature trees to infection by the mountain pine beetle fungal associate, Grosmannia clavigera. Tree Physiol. 2014;34:1220–1239. doi: 10.1093/treephys/tpt101. PubMed DOI PMC
Ayres MP, Lombardero MJ. Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Sci Total Environ. 2000;262:263–286. doi: 10.1016/S0048-9697(00)00528-3. PubMed DOI
Baier P, Führer E, Kirisits T, Rosner S. Defence reactions of Norway spruce against bark beetles and the associated fungus Ceratocystis polonica in secondary pure and mixed species stands. Forest Ecol Manag. 2002;159:73–86. doi: 10.1016/S0378-1127(01)00711-3. DOI
Bakke A. Spruce bark beetle, Ips typographus: Pheromone production and field response to synthetic pheromones. Naturwissenschaften. 1976;63:92. doi: 10.1007/bf00622413. PubMed DOI
Bakke A. Inhibition of the response in Ips typographus to the aggregation pheromone; field evaluation of verbenone and ipsenol. Z Angew Entomol. 1981;92:172–177. doi: 10.1111/j.1439-0418.1981.tb01666.x. DOI
Balogh SL, Huber DPW, Lindgren BS. Single-generation effects on terpenoid defenses in lodgepole pine populations following mountain pine beetle infestation. PLoS One. 2018;13:e0196063. doi: 10.1371/journal.pone.0196063. PubMed DOI PMC
Bansal S, Germino MJ. Temporal variation of nonstructural carbohydrates in montane conifers: similarities and differences among developmental stages, species and environmental conditions. Tree Physiol. 2009;29:559–568. doi: 10.1093/treephys/tpn045. PubMed DOI
Bentz B, Six DL. Ergosterol content of fungi associated with Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera: Curculionidae, Scolytinae) Ann Entomol Soc Am. 2006;99:189–194. doi: 10.1603/0013-8746(2006)099[0189:ECOFAW]2.0.CO;2. DOI
Bentz BJ, Jönsson AM, Schroeder M, Weed A, Wilcke RAI, Larsson K. Ips typographus and Dendroctonus ponderosae models project thermal suitability for intra- and inter-continental establishment in a changing climate. Front For Glob. 2019;2:1. doi: 10.3389/ffgc.2019.00001. DOI
Berini JL, Brockman SA, Hegeman AD, Reich PB, Muthukrishnan R, Montgomery RA, Forester JD. Combinations of abiotic factors differentially alter production of plant secondary metabolites in five woody plant species in the boreal-temperate transition zone. Front Plant Sci. 2018;9:1257. doi: 10.3389/fpls.2018.01257. PubMed DOI PMC
Berryman AA. Resistance of conifers to invasion by bark beetle-fungus associations. Bioscience. 1972;22:598–602. doi: 10.2307/1296206%JBioScience. DOI
Biedermann PHW, Muller J, Grégoire J-C, et al. Bark beetle population dynamics in the anthropocene: challenges and solutions. Trends Ecol Evol. 2019;34:914–924. doi: 10.1016/j.tree.2019.06.002. PubMed DOI
Binyameen M, Jankuvová J, Blaženec M, et al. Co-localization of insect olfactory sensory cells improves the discrimination of closely separated odour sources. Funct Ecol. 2014;28:1216–1223. doi: 10.1111/1365-2435.12252. DOI
Birgersson G, Bergström G. Volatiles released from individual spruce bark beetle entrance holes: quantitative variations during the first week of attack. J Chem Ecol. 1989;15:2465–2483. doi: 10.1007/BF01020377. PubMed DOI
Birgersson G, Schlyter F, Löfqvist J, Bergström G. Quantitative variation of pheromone components in the spruce bark beetle Ips typographus from different attack phases. J Chem Ecol. 1984;10:1029–1055. doi: 10.1007/BF00987511. PubMed DOI
Blažytė-Čereškienė L, Apšegaitė V, Radžiutė S, Mozūraitis R, Būda V, Pečiulytė D. Electrophysiological and behavioural responses of Ips typographus (L.) to trans-4-thujanol—a host tree volatile compound. Ann For Sci. 2015;73:247–256. doi: 10.1007/s13595-015-0494-5. DOI
Blomquist GJ, Figueroa-Teran R, Aw M, et al. Pheromone production in bark beetles. Insect Biochem Mol Biol. 2010;40:699–712. doi: 10.1016/j.ibmb.2010.07.013. PubMed DOI
Blomqvist M, Kosunen M, Starr M, Kantola T, Holopainen M, Lyytikäinen-Saarenmaa P. Modelling the predisposition of Norway spruce to Ips typographus L. infestation by means of environmental factors in southern Finland. Eur J For Res. 2018;137:675–691. doi: 10.1007/s10342-018-1133-0. DOI
Borg-Karlson AK, Lindström M, Norin T, Persson M, Valterová I. Enantiomeric composition of monoterpene hydrocarbons in different tissues of Norway spruce, Picea abies (L) Karst. A multi-dimensional gas chromatography study. Acta Chem Scand. 1993;47:138–144. doi: 10.3891/acta.chem.scand.47-0138. DOI
Branco M, Pereira JS, Mateus E, Tavares C, Paiva MR. Water stress affects Tomicus destruens host pine preference and performance during the shoot feeding phase. Ann For Sci. 2010;67:608–608. doi: 10.1051/forest/201021. DOI
Brignolas F, Lacroix B, Lieutier F, et al. lnduced responses in phenolic metabolism in two Norway spruce clones after wounding and inoculations with Ophiostoma polonicum, a bark beetle-associated fungus. Plant Physiol. 1995;109:821–827. doi: 10.1104/pp.109.3.821. PubMed DOI PMC
Brignolas F, Lieutier F, Sauvard D, Christiansen E, Berryman AA. Phenolic predictors for Norway spruce resistance to the bark beetle Ips typographus (Coleoptera: Scolytidae) and an associated fungus, Ceratocystis polonica. Can J For Res. 1998;28:720–728. doi: 10.1139/x98-037. DOI
Bruce TJA, Pickett JA. Perception of plant volatile blends by herbivorous insects – Finding the right mix. Phytochemistry. 2011;72:1605–1611. doi: 10.1016/j.phytochem.2011.04.011. PubMed DOI
Bryant JP, Chapin FS, Klein DR. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos. 1983;40:357–368. doi: 10.2307/3544308. DOI
Byers JA. Chemical ecology of bark beetles. Experientia. 1989;45:271–283. doi: 10.1007/bf01951813. DOI
Byers JA. Effects of attraction radius and flight paths on catch of scolytid beetles dispersing outward through rings of pheromone traps. J Chem Ecol. 1999;25:985–1005. doi: 10.1023/A:1020869422943. DOI
Byers JA. Wind-aided dispersal of simulated bark beetles flying through forests. Ecol Model. 2000;125:231–243. doi: 10.1016/S0304-3800(99)00187-8. DOI
Byers JA, Birgersson G. Pheromone production in a bark beetle independent of myrcene precursor in host pine species. Naturwissenschaften. 1990;77:385–387. doi: 10.1007/bf01135739. DOI
Byers JA, Zhang Q-H, Schlyter F, Birgersson G. Volatiles from nonhost birch trees inhibit pheromone response in spruce bark beetles. Naturwissenschaften. 1998;85:557–561. doi: 10.1007/s001140050551. DOI
Byers JA, Zhang QH, Birgersson G. Strategies of a bark beetle, Pityogenes bidentatus, in an olfactory landscape. Naturwissenschaften. 2000;87:503–507. doi: 10.1007/s001140050768. PubMed DOI
Caldeira MC. The timing of drought coupled with pathogens may boost tree mortality. Tree Physiol. 2019;39:1–5. doi: 10.1093/treephys/tpy141. PubMed DOI
Cale JA, Ding R, Wang F, Rajabzadeh R, Erbilgin N. Ophiostomatoid fungi can emit the bark beetle pheromone verbenone and other semiochemicals in media amended with various pine chemicals and beetle-released compounds. Fungal Ecol. 2019;39:285–295. doi: 10.1016/j.funeco.2019.01.003. DOI
Celedon JM, Bohlmann J. Oleoresin defenses in conifers: chemical diversity, terpene synthases and limitations of oleoresin defense under climate change. New Phytol. 2019;224:1444–1463. doi: 10.1111/nph.15984. PubMed DOI
Chakraborty A, Ashraf MZ, Modlinger R, Synek J, Schlyter F, Roy A. Unravelling the gut bacteriome of Ips (Coleoptera: Curculionidae: Scolytinae): identifying core bacterial assemblage and their ecological relevance. Sci Rep. 2020;10:18572. doi: 10.1038/s41598-020-75203-5. PubMed DOI PMC
Chakraborty A, Modlinger R, Ashraf MZ, Synek J, Schlyter F, Roy A. Core mycobiome and their ecological relevance in the gut of five Ips bark beetles (Coleoptera: Curculionidae: Scolytinae) Front Microbiol. 2020;11:568853. doi: 10.3389/fmicb.2020.568853. PubMed DOI PMC
Chang R, Duong TA, Taerum SJ, Wingfield MJ, Zhou X, Yin M, de Beer ZW. Ophiostomatoid fungi associated with the spruce bark beetle Ips typographus, including 11 new species from China. Persoonia. 2019;42:50–74. doi: 10.3767/persoonia.2019.42.03. PubMed DOI PMC
Chong J, Poutaraud A, Hugueney P. Metabolism and roles of stilbenes in plants. Plant Sci. 2009;177:143–155. doi: 10.1016/j.plantsci.2009.05.012. DOI
Christiansen E, Glosli AM (1996) Mild drought enhances the resistance of Norway spruce to a bark beetle-transmitted blue-stain fungus. vol NC-183. USDA Forest Service Gen. Tech. Rep., St. Paul, MN 55108
Christiansen E, Waring RH, Berryman AA. Resistance of conifers to bark beetle attack: searching for general relationships. For Ecol Manag. 1987;22:89–106. doi: 10.1016/0378-1127(87)90098-3. DOI
Coulson RN, Pulley PE, Pope DN, Fargo WS, Gagne JA, Kelly CL (1980) Estimation of survival and allocation of adult southern pine beetles between trees during the development of an infestation. In: Berryman AA, Safranyik L (eds) Proceedings of the second IUFRO conference on dispersal of forest insects: evaluation, theory and management implications. Washington State University, Pullman, USA, Sandpoint, Idaho, USA, pp 194–212
Croisé L, Lieutier F, Cochard H, Dreyer E. Effects of drought stress and high density stem inoculations with Leptographium wingfieldii on hydraulic properties of young Scots pine trees. Tree Physiol. 2001;21:427–436. doi: 10.1093/treephys/21.7.427. PubMed DOI
Davis TS. The ecology of yeasts in the bark beetle holobiont: a century of research revisited. Microb Ecol. 2015;69:723–732. doi: 10.1007/s00248-014-0479-1. PubMed DOI
Davis TS, Stewart JE, Mann A, Bradley C, Hofstetter R. Evidence for multiple ecological roles of Leptographium abietinum, a symbiotic fungus associated with the North American spruce beetle. Fungal Ecol. 2019;38:62–70. doi: 10.1016/j.funeco.2018.04.008. DOI
Devkota P, Enebak SA, Eckhardt LG. The impact of drought and vascular-inhabiting pathogen invasion in Pinus taeda health. Int J For Res. 2018;2018:1–9. doi: 10.1155/2018/1249140. DOI
Dickens JC. Behavioural and electro-physiological responses of the bark beetle Ips typographus to potential pheromone components. Physiol Entomol. 1981;6:251–261. doi: 10.1111/j.1365-3032.1981.tb00269.x. DOI
Eldhuset TD, Nagy NE, Volařík D, Børja I, Gebauer R, Yakovlev IA, Krokene P. Drought affects tracheid structure, dehydrin expression, and above- and belowground growth in 5-year-old Norway spruce. Plant Soil. 2013;366:305–320. doi: 10.1007/s11104-012-1432-z. DOI
Elkinton JS, Wood DL. Feeding and boring behavior of the bark beetle Ips paraconfusus (Coleoptera: Scolytidae) on the bark of a host and non-host tree species. Can Entomol. 1980;112:797–809. doi: 10.4039/Ent112797-8. DOI
Erbilgin N, Krokene P, Christiansen E, Zeneli G, Gershenzon J. Exogenous application of methyl jasmonate elicits defenses in Norway spruce (Picea abies) and reduces host colonization by the bark beetle Ips typographus. Oecologia. 2006;148:426–436. doi: 10.1007/s00442-006-0394-3. PubMed DOI
Erbilgin N, Krokene P, Kvamme T, Christiansen E. A host monoterpene influences Ips typographus (Coleoptera: Curculionidae, Scolytinae) responses to its aggregation pheromone. Agr For Entomol. 2007;9:135–140. doi: 10.1111/j.1461-9563.2007.00329.x. DOI
Erbilgin N, Cale JA, Hussain A, Ishangulyyeva G, Klutsch JG, Najar A, Zhao S. Weathering the storm: how lodgepole pine trees survive mountain pine beetle outbreaks. Oecologia. 2017;184:469–478. doi: 10.1007/s00442-017-3865-9. PubMed DOI
Evensen PC, Solheim H, Høiland K, Stenersen J. Induced resistance of Norway spruce, variation of phenolic compounds and their effects on fungal pathogens. For Pathol. 2000;30:97–108. doi: 10.1046/j.1439-0329.2000.00189.x. DOI
Everaerts C, Grégoire JC, Merlin J. The toxicity of Norway spruce monoterpenes to two bark beetle species and their associates. In: Mattson WJ, Levieux J, Bernard-Dagan C, editors. Mechanisms of woody plant defences against insects. Search for pattern. Berlin: Springer; 1988. pp. 335–344.
Eyles A, Bonello P, Ganley R, Mohammed C. Induced resistance to pests and pathogens in trees. New Phytol. 2010;185:893–908. doi: 10.1111/j.1469-8137.2009.03127.x. PubMed DOI
Faccoli M, Schlyter F. Conifer phenolic resistance markers are bark beetle antifeedant semiochemicals. Agr For Entomol. 2007;9:237–245. doi: 10.1111/j.1461-9563.2007.00339.x. DOI
Faccoli M, Blazenec M, Schlyter F. Feeding response to host and nonhost compounds by males and females of the spruce bark beetle Ips typographus in a tunneling microassay. J Chem Ecol. 2005;31:745–759. doi: 10.1007/s10886-005-3542-z. PubMed DOI
Felicijan M, Novak M, Kraševec N, Urbanek Krajnc A. Antioxidant defences of Norway spruce bark against bark beetles and its associated blue-stain fungus. Agricultura. 2015;12:9–18. doi: 10.1515/agricultura-2016-0002. DOI
Felicijan M, Kristl J, Krajnc AU. Pre-treatment with salicylic acid induces phenolic responses of Norway spruce (Picea abies) bark to bark beetle (Ips typographus) attack. Trees. 2016;30:2117–2129. doi: 10.1007/s00468-016-1438-x. DOI
Ferrenberg S, Kane JM, Langenhan JM. To grow or defend? Pine seedlings grow less but induce more defences when a key resource is limited. Tree Physiol. 2015;35:107–111. doi: 10.1093/treephys/tpv015. PubMed DOI
Ferrenberg S, Langenhan JM, Loskot SA, Rozal LM, Mitton JB. Resin monoterpene defenses decline within three widespread species of pine (Pinus) along a 1530-m elevational gradient. Ecosphere. 2017;8:e01975. doi: 10.1002/ecs2.1975. DOI
Fossdal CG, Nagy NE, Johnsen O, Dalen LS. Local and systemic stress responses in Norway spruce: similarities in gene expression between a compatible pathogen interaction and drought stress. Physiol Mol Plant P. 2007;70:161–173. doi: 10.1016/j.pmpp.2007.09.002. DOI
Franceschi VR, Krokene P, Krekling T, Christiansen E. Phloem parenchyma cells are involved in local and distant defense responses to fungal inoculation or bark-beetle attack in Norway spruce (Pinaceae) Am J Bot. 2000;87:314–326. doi: 10.2307/2656627. PubMed DOI
Franceschi VR, Krokene P, Christiansen E, Krekling T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol. 2005;167:353–375. doi: 10.1111/j.1469-8137.2005.01436.x. PubMed DOI
Francke W, Vité JP. Oxygenated terpenes in pheromone systems of bark beetles. J Appl Entomol. 1983;96:146–156. doi: 10.1111/j.1439-0418.1983.tb03655.x. DOI
Franklin AJ, Debruyne C, Grégoire J-C. Recapture of Ips typographus L. (Col., Scolytidae) with attractants of low release rates: localized dispersion and environmental influences. Agr For Entomol. 2000;2:259–270. doi: 10.1046/j.1461-9563.2000.00075.x. DOI
Gaylord ML, Kolb TE, Pockman WT, et al. Drought predisposes pinon-juniper woodlands to insect attacks and mortality. New Phytol. 2013;198:567–578. doi: 10.1111/nph.12174. PubMed DOI
Gely C, Laurance SGW, Stork NE. How do herbivorous insects respond to drought stress in trees? Biol Rev Camb Philos Soc. 2020;95:434–448. doi: 10.1111/brv.12571. PubMed DOI
Ghimire RP, Kivimäenpää M, Blomqvist M, Holopainen T, Lyytikäinen-Saarenmaa P, Holopainen JK. Effect of bark beetle (Ips typographus L.) attack on bark VOC emissions of Norway spruce (Picea abies Karst.) trees. Atmos Environ. 2016;126:145–152. doi: 10.1016/j.atmosenv.2015.11.049. DOI
Graham K. Release by flight exercise of a chemotropic response from photopositive domination in a scolytid beetle. Nature. 1959;184:283–284. doi: 10.1038/184283b0. DOI
Grossiord C. Having the right neighbors: how tree species diversity modulates drought impacts on forests. New Phytol. 2019 doi: 10.1111/nph.15667. PubMed DOI
Hallberg E. Sensory organs in Ips typographus (Insecta: Coleoptera)—fine structure of the sensilla of the maxillary and labial palps. Acta Zool. 1982;63:191–198. doi: 10.1111/j.1463-6395.1982.tb00778.x. DOI
Hammerbacher A, Ralph SG, Bohlmann J, Fenning TM, Gershenzon J, Schmidt A. Biosynthesis of the major tetrahydroxystilbenes in spruce, astringin and isorhapontin, proceeds via resveratrol and is enhanced by fungal infection. Plant Physiol. 2011;157:876–890. doi: 10.1104/pp.111.181420. PubMed DOI PMC
Hammerbacher A, Schmidt A, Wadke N, et al. A common fungal associate of the spruce bark beetle metabolizes the stilbene defenses of Norway spruce. Plant Physiol. 2013;162:1324–1336. doi: 10.1104/pp.113.218610. PubMed DOI PMC
Hammerbacher A, Paetz C, Wright LP, et al. Flavan-3-ols in Norway spruce: biosynthesis, accumulation, and function in response to attack by the bark beetle-associated fungus Ceratocystis polonica. Plant Physiol. 2014;164:2107–2122. doi: 10.1104/pp.113.232389. PubMed DOI PMC
Hammerbacher A, Raguschke B, Wright LP, Gershenzon J. Gallocatechin biosynthesis via a flavonoid 3',5'-hydroxylase is a defense response in Norway spruce against infection by the bark beetle-associated sap-staining fungus Endoconidiophora polonica. Phytochemistry. 2018;148:78–86. doi: 10.1016/j.phytochem.2018.01.017. PubMed DOI
Hammerbacher A, Kandasamy D, Ullah C, Schmidt A, Wright LP, Gershenzon J. Flavanone-3-Hydroxylase plays an important role in the biosynthesis of spruce phenolic defenses against bark beetles and their fungal associates. Front Plant Sci. 2019;10:208. doi: 10.3389/fpls.2019.00208. PubMed DOI PMC
Hansson BS, Anton S. Function and morphology of the antennal lobe: new developments. Annu Rev Entomol. 2000;45:203–231. doi: 10.1146/annurev.ento.45.1.203. PubMed DOI
Hansson BS, Stensmyr MC. Evolution of insect olfaction. Neuron. 2011;72:698–711. doi: 10.1016/j.neuron.2011.11.003. PubMed DOI
Hartmann H, Moura CF, Anderegg WRL, et al. Research frontiers for improving our understanding of drought induced tree and forest mortality. New Phytol. 2018;218:15–28. doi: 10.1111/nph.15048. PubMed DOI
Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. Q Rev Biol. 1992;67:283–335. doi: 10.1086/417659. DOI
Hietz P, Baier P. Tree temperatures, volatile organic emissions, and primary attraction of bark beetles. Phyton Ann Rei Bot A. 2005;45(3):341.
Hoch G, Richter A, Körner C. Non-structural carbon compounds in temperate forest trees. Plant Cell Environ. 2003;26:1067–1081. doi: 10.1046/j.0016-8025.2003.01032.x. DOI
Holopainen JK, Virjamo V, Ghimire RP, Blande JD, Julkunen-Tiitto R, Kivimaenpaa M. Climate change effects on secondary compounds of forest trees in the Northern hemisphere. Front Plant Sci. 2018;9:1445. doi: 10.3389/fpls.2018.01445. PubMed DOI PMC
Huang J, Hammerbacher A, Weinhold A, et al. Eyes on the future - evidence for trade-offs between growth, storage and defense in Norway spruce. New Phytol. 2019;222:144–158. doi: 10.1111/nph.15522. PubMed DOI
Huang J, Kautz M, Trowbridge AM, et al. Tree defence and bark beetles in a drying world: carbon partitioning, functioning and modelling. New Phytol. 2020;225:26–36. doi: 10.1111/nph.16173. PubMed DOI
Hussain A, Classens G, Guevara-Rozo S, Cale JA, Rajabzadeh R, Peters BR, Erbilgin N. Spatial variation in soil available water holding capacity alters carbon mobilization and allocation to chemical defenses along jack pine stems. Environ Exp Bot. 2020 doi: 10.1016/j.envexpbot.2019.103902. DOI
Ishangulyyeva G, Najar A, Curtis JM, Erbilgin N. Fatty acid composition of novel host jack pine do not prevent host acceptance and colonization by the invasive mountain pine beetle and its symbiotic fungus. PLoS One. 2016;11(9):1–21. doi: 10.1371/journal.pone.016204610.7939/DVN/10836. PubMed DOI PMC
Jackson GE, Irvine J, Grace J, Khalil AAM. Abscisic acid concentrations and fluxes in droughted conifer saplings. Plant Cell Environ. 1995;18:13–22. doi: 10.1111/j.1365-3040.1995.tb00539.x. DOI
Jacquet JS, Bosc A, O'Grady A, Jactel H. Combined effects of defoliation and water stress on pine growth and non-structural carbohydrates. Tree Physiol. 2014;34:367–376. doi: 10.1093/treephys/tpu018. PubMed DOI
Jactel H, Petit J, Desprez-Loustau M-L, Delzon S, Piou D, Battisti A, Koricheva J. Drought effects on damage by forest insects and pathogens: a meta-analysis. Glob Change Biol. 2012;18:267–276. doi: 10.1111/j.1365-2486.2011.02512.x. DOI
Jakoby O, Lischke H, Wermelinger B. Climate change alters elevational phenology patterns of the European spruce bark beetle (Ips typographus) Glob Change Biol. 2019;25:4048–4063. doi: 10.1111/gcb.14766. PubMed DOI
Jakuš R, Edwards-Jonášová M, Cudlín P, Blaženec M, Ježík M, Havlíček F, Moravec I. Characteristics of Norway spruce trees (Picea abies) surviving a spruce bark beetle (Ips typographus L.) outbreak. Trees. 2011;25:965–973. doi: 10.1007/s00468-011-0571-9. DOI
Kainulainen PJ, Oksanen J, Palomäki V, Holopainen JK, Holopainen T. Effect of drought and waterlogging stress on needle monoterpenes of Picea abies. Can J Bot. 1992;70:1613–1616. doi: 10.1139/b92-203. DOI
Kalinová B, Brizova R, Knizek M, Turcani M, Hoskovec M. Volatiles from spruce trap-trees detected by Ips typographus bark beetles: chemical and electrophysiological analyses. Arthropod Plant Interact. 2014;8:305–316. doi: 10.1007/s11829-014-9310-7. DOI
Kandasamy D, Gershenzon J, Hammerbacher A. Volatile organic compounds emitted by fungal associates of conifer bark beetles and their potential in bark beetle control. J Chem Ecol. 2016;42:952–969. doi: 10.1007/s10886-016-0768-x. PubMed DOI PMC
Kandasamy D, Gershenzon J, Andersson MN, Hammerbacher A. Volatile organic compounds influence the interaction of the Eurasian spruce bark beetle (Ips typographus) with its fungal symbionts. ISME J. 2019;13:1788–1800. doi: 10.1038/s41396-019-0390-3. PubMed DOI PMC
Kännaste A, Zhao T, Lindström A, Stattin E, Långström B, Borg-Karlson A-K. Odors of Norway spruce (Picea abies L.) seedlings: differences due to age and chemotype. Trees. 2012;27:149–159. doi: 10.1007/s00468-012-0783-7. DOI
Kausrud KL, Grégoire J-C, Skarpaas O, Erbilgin N, Gilbert M, Økland B, Stenseth NC. Trees Wanted—Dead or Alive! Host selection and population dynamics in tree-killing bark beetles. PLoS One. 2011;6:e18274. doi: 10.1371/journal.pone.0018274. PubMed DOI PMC
Kausrud K, Økland B, Skarpaas O, Grégoire J-C, Erbilgin N, Stenseth NC. Population dynamics in changing environments: the case of an eruptive forest pest species. Bio Rev. 2012;87:34–51. doi: 10.1111/j.1469-185X.2011.00183.x. PubMed DOI
Kelsey RG, Gallego D, Sánchez-García FJ, Pajares JA. Ethanol accumulation during severe drought may signal tree vulnerability to detection and attack by bark beetles. Can J For Res. 2014;44:554–561. doi: 10.1139/cjfr-2013-0428. DOI
Kirisits T. 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, editors. Bark and wood boring insects in living trees in Europe, a synthesis. Dordrecht: Springer; 2004. pp. 181–236.
Klutsch JG, Shamoun SF, Erbilgin N. Drought stress leads to systemic induced susceptibility to a nectrotrophic fungus associated with mountain pine beetle in Pinus banksiana seedlings. PLoS One. 2017;12:e0189203. doi: 10.1371/journal.pone.0189203. PubMed DOI PMC
Kohnle U, Vité JP, Baader EJ, Meyer H, Francke W. Chirality of ipsdienol and ipsenol indicates a frass pheromone system in the spruce engraver, Ips typographus. Naturwissenschaften. 1991;78:136–138. doi: 10.1007/BF01131493. DOI
Kolb TE, Fettig CJ, Ayres MP, et al. Observed and anticipated impacts of drought on forest insects and diseases in the United States. For Ecol Manag. 2016;380:321–334. doi: 10.1016/j.foreco.2016.04.051. DOI
Kolb T, Keefover-Ring K, Burr SJ, Hofstetter R, Gaylord M, Raffa KF. Drought-mediated changes in tree physiological processes weaken tree defenses to bark beetle attack. J Chem Ecol. 2019;45:888–890. doi: 10.1007/s10886-019-01105-0. PubMed DOI
Koricheva J, Larsson S, Haukioja E, Keinänen M. Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos. 1998;83:212–226. doi: 10.2307/3546833. DOI
Körner C. Carbon limitation in trees. J Ecol. 2003;91:4–17. doi: 10.1046/j.1365-2745.2003.00742.x. DOI
Krokene P. Conifer defense and resistance to bark beetles. In: Vega FE, Hofstetter R, editors. Bark beetles: biology and ecology of native and invasive species. Cambridge: Academic Press; 2015. pp. 177–207.
Krokene P, Solheim H, Christiansen E. Induction of disease resistance in Norway spruce (Picea abies) by necrotizing fungi. Plant Pathol. 2001;50:230–233. doi: 10.1046/j.1365-3059.2001.00559.x. DOI
Lahr EC, Krokene P. Conifer stored resources and resistance to a fungus associated with the spruce bark beetle Ips typographus. PLoS One. 2013;8:e72405. doi: 10.1371/journal.pone.0072405. PubMed DOI PMC
Leufvén A, Birgersson G. Quantitative variation of different monoterpenes around galleries of Ips typographus (Coleoptera:Scolytidae) attacking Norway spruce. Can J Bot. 1987;65:1038–1044. doi: 10.1139/b87-144. DOI
Leufvén A, Bergström G, Falsen E. Interconversion of verbenols and verbenone by identified yeasts isolated from the spruce bark beetle Ips typographus. J Chem Ecol. 1984;10:1349–1361. doi: 10.1007/BF00988116. PubMed DOI
Leufvén A, Bergström G, Falsen E. Oxygenated monoterpenes produced by yeasts, isolated from Ips typographus (Coleoptera: Scolytidae) and grown in phloem medium. J Chem Ecol. 1988;14:353–362. doi: 10.1007/BF01022551. PubMed DOI
Lewinsohn E, Gijzen M, Muzika RM, Barton K, Croteau RB. Oleoresinosis in Grand fir (Abies grandis) saplings and mature trees. Plant Physiol. 1993;101:1021–1028. doi: 10.1104/pp.101.3.1021. PubMed DOI PMC
Li SH, Nagy NE, Hammerbacher A, Krokene P, Niu XM, Gershenzon J, Schneider B. Localization of phenolics in phloem parenchyma cells of Norway spruce (Picea abies) Chembiochem Eur J Chem Biol. 2012;13:2707–2713. doi: 10.1002/cbic.201200547. PubMed DOI
Lieutier F. Host resistance to bark beetles and its variations. In: Lieutier F, Day KR, Battisti A, Grégoire J-C, Evans HF, editors. Bark and wood boring insects in living trees in Europe - A Synthesis. Dordrecht: Springer; 2004. p. 569.
Lieutier F, Brignolas F, Sauvard D, Yart A, Galet C, Brunet M, Van de Sype H. Intra- and inter-provenance variability in phloem phenols of Picea abies and relationship to a bark beetle-associated fungus. Tree Physiol. 2003;23:247–256. doi: 10.1093/treephys/23.4.247. PubMed DOI
Lieutier F, Yart A, Salle A. Stimulation of tree defenses by ophiostomatoid fungi can explain attack success of bark beetles on conifers. Ann For Sci. 2009;66:801. doi: 10.1051/forest/2009066. DOI
Lindelöw Å, Risberg B, Sjödin K. Attraction during flight of scolytids and other bark-and wood-dwelling beetles to volatiles from fresh and stored spruce wood. Can J For Res. 1992;22:224–228. doi: 10.1139/x92-029. DOI
Lindgren BS, Miller DR. Effect of verbenone on five species of bark beetles (Coleoptera:Scolytidae) in lodgepole pine forests. Environ Entomol. 2019;31:759–765. doi: 10.1603/0046-225X-31.5.759. DOI
Lindgren BS, Raffa KF. Evolution of tree killing in bark beetles (Coleoptera: Curculionidae): trade-offs between the maddening crowds and a sticky situation. Can Entomol. 2013;145:471–495. doi: 10.4039/tce.2013.27. DOI
Lindström M, Norin T, Birgersson G, Schlyter F. Variation of enantiomeric composition of alpha-pinene in Norway spruce, Picea abies, and its influence on production of verbenol isomers by Ips typographus in the field. J Chem Ecol. 1989;15:541–548. doi: 10.1007/BF01014699. PubMed DOI
Linnakoski R, de Beer ZW, Niemela P, Wingfield MJ. Associations of conifer-infesting bark beetles and fungi in Fennoscandia. Insects. 2012;3:200–227. doi: 10.3390/insects3010200. PubMed DOI PMC
Linnakoski R, Sugano J, Junttila S, Pulkkinen P, Asiegbu FO, Forbes KM. Effects of water availability on a forestry pathosystem: fungal strain-specific variation in disease severity. Sci Rep. 2017;7:13501. doi: 10.1038/s41598-017-13512-y. PubMed DOI PMC
Lombardero MJ, Ayres MP, Lorio PL, Ruel JJ. Environmental effects on constitutive and inducible resin defences of Pinus taeda. Ecol Lett. 2000;3:329–339. doi: 10.1046/j.1461-0248.2000.00163.x. DOI
Lopez-Goldar X, Villari C, Bonello P, Borg-Karlson AK, Grivet D, Zas R, Sampedro L. Inducibility of plant secondary metabolites in the stem predicts genetic variation in resistance against a key insect herbivore in maritime pine. Front Plant Sci. 2018;9:1651. doi: 10.3389/fpls.2018.01651. PubMed DOI PMC
Lusebrink I, Erbilgin N, Evenden ML. The effect of water limitation on volatile emission, tree defense response, and brood success of Dendroctonus ponderosae in two pine hosts, Lodgepole, and Jack pine. Front Ecol Evol. 2016 doi: 10.3389/fevo.2016.00002. DOI
Mageroy MH, Wilkinson SW, Tengs T, et al. Molecular underpinnings of methyl jasmonate-induced resistance in Norway spruce. Plant Cell Environ. 2020 doi: 10.1111/pce.13774. PubMed DOI
Månsson PE (2005) Host selection and antifeedants in Hylobius abietis pine weevils. Dissertation, Swedish University of Agricultural Sciences
Marin M, Preisig O, Wingfield BD, Kirisits T, Yamaoka Y, Wingfield MJ. Phenotypic and DNA sequence data comparisons reveal three discrete species in the Ceratocystis polonica species complex. Mycol Res. 2005;109:1137–1148. doi: 10.1017/S095375620500362X. PubMed DOI
Marini L, Økland B, Jönsson AM, et al. Climate drivers of bark beetle outbreak dynamics in Norway spruce forests. Ecography. 2017;40:1426–1435. doi: 10.1111/ecog.02769. DOI
Martin D, Tholl D, Gershenzon J, Bohlmann J. Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway Spruce stems. Plant Physiol. 2002;129:1003. doi: 10.1104/pp.011001. PubMed DOI PMC
Martin DM, Gershenzon J, Bohlmann J. Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway Spruce. Plant Physiol. 2003;132:1586–1599. doi: 10.1104/pp.103.021196. PubMed DOI PMC
Mattson WJ, Haak RA. The role of drought in outbreaks of plant-eating insects. Drought's physiological effects on plants can predict its influence on insect populations. Bioscience. 1987;37:110–118. doi: 10.2307/1310365. DOI
McDowell NG. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol. 2011;155:1051–1059. doi: 10.1104/pp.110.170704. PubMed DOI PMC
McDowell N, Sevanto S. The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytol. 2010;186:264–266. doi: 10.1111/j.1469-8137.2010.03232.x. PubMed DOI
McDowell N, Pockman WT, Allen CD, et al. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol. 2008;178:719–739. doi: 10.1111/j.1469-8137.2008.02436.x. PubMed DOI
Merker E. Die Abhängigkeit des biologischen Gleichgewichts des Großen Fichtenborkenkäfers vom Wasserhaushalt des Waldes - Dependency of biological equilibrium of the European spruce bark beetle from forest water supply. Waldhygiene. 1956;1:173–187.
Messner B, Schröder P. Burst amplifying system in cell suspension cultures of spruce (Picea abies L. Karst.): Modulation of elicitor-induced release of hydrogen peroxide (oxidative burst) by ionophores and salicylic acid. J Appl Bot Food Qual. 1999;73:6–10.
Metsämuuronen S, Sirén H. Bioactive phenolic compounds, metabolism and properties: a review on valuable chemical compounds in Scots pine and Norway spruce. Phytochem Rev. 2019;18:623–664. doi: 10.1007/s11101-019-09630-2. DOI
Moran E, Lauder J, Musser C, Stathos A, Shu M. The genetics of drought tolerance in conifers. New Phytol. 2017;216:1034–1048. doi: 10.1111/nph.14774. PubMed DOI
Mustaparta H, Tømmerås BÅ, Baeckström P, Bakke JM, Ohloff G. Ipsdienol-specific receptor cells in bark beetles: structure-activity relationships of various analogues and of deuterium-labelled ipsdienol. J Comp Physiol A. 1984;154:591–595. doi: 10.1007/BF00610172. DOI
Nagy NE, Fossdal CG, Krokene P, Krekling T, Lönneborg A, Solheim H. Induced responses to pathogen infection in Norway spruce phloem:changes in polyphenolic parenchyma cells, chalcone synthasetranscript levels and peroxidase activity. Tree Physiol. 2004;24:505–515. doi: 10.1093/treephys/24.5.505. PubMed DOI
Netherer S, Matthews B, Katzensteiner K, et al. Do water-limiting conditions predispose Norway spruce to bark beetle attack? New Phytol. 2015;205:1128–1141. doi: 10.1111/nph.13166. PubMed DOI PMC
Netherer S, Ehn M, Blackwell E, Kirisits T. Defence reactions of mature Norway spruce (Picea abies) before and after inoculation of the blue-stain fungus Endoconidiophora polonica in a drought stress experiment. Cent Eur For. 2016;62:169–177. doi: 10.1515/forj-2016-0014. DOI
Netherer S, Panassiti B, Pennerstorfer J, Matthews B. Acute drought is an important driver of bark beetle infestation in Austrian Norway spruce stands. Front For Glob Change. 2019 doi: 10.3389/ffgc.2019.00039. DOI
Niinemets Ü. Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. Forest Ecol Manag. 2010;260:1623–1639. doi: 10.1016/j.foreco.2010.07.054. DOI
Novak M, Krajnc AU, Lah L, et al. Low-density Ceratocystis polonica inoculation of Norway spruce (Picea abies) triggers accumulation of monoterpenes with antifungal properties. Eur J For Res. 2013;133:573–583. doi: 10.1007/s10342-013-0772-4. DOI
Ormeno E, Mevy JP, Vila B, Bousquet-Melou A, Greff S, Bonin G, Fernandez C. Water deficit stress induces different monoterpene and sesquiterpene emission changes in Mediterranean species. Relationship between terpene emissions and plant water potential. Chemosphere. 2007;67:276–284. doi: 10.1016/j.chemosphere.2006.10.029. PubMed DOI
Pentzold S, Burse A, Boland W. Contact chemosensation of phytochemicals by insect herbivores. Nat Prod Rep. 2017;34:478–483. doi: 10.1039/C7NP00002B. PubMed DOI PMC
Persson M, Sjödin K, Borg-Karlson AK, Norin T, Ekberg I. Relative amounts and enantiomeric compositions of monoterpene hydrocarbons in xylem and needles of Picea abies. Phytochemistry. 1996 doi: 10.1016/0031-9422(96)00119-7. DOI
Petterson EM, Boland W. Potential parasitoid attractants, volatile composition throughout a bark beetle attack. Chemoecology. 2003;13:27–37. doi: 10.1007/s000490300003. DOI
Popa V, Déziel E, Lavallée R, Bauce E, Guertin C. The complex symbiotic relationships of bark beetles with microorganisms: a potential practical approach for biological control in forestry. Pest Manag Sci. 2012;68:963–975. doi: 10.1002/ps.3307. PubMed DOI
Powell D, Groβe-Wilde E, Krokene P, et al. A highly contiguous genome assembly of a major forest pest, the Eurasian spruce bark beetle Ips typographus. BioRxiv. 2020 doi: 10.1101/2020.11.28.401976. PubMed DOI PMC
Raffa KF, Grégoire JC, Lindgren BS. Natural history and ecology of bark beetles. In: Vega FE, Hofstetter RW, editors. Bark beetles Biology and ecology of native and invasive species. Cambridhe: Academic Press; 2015. pp. 1–40.
Raffa KF, Andersson MN, Schlyter F. Host selection by bark beetles: playing the odds in a high-stake game. Adv Insect Physiol. 2016;50:1–74. doi: 10.1016/bs.aiip.2016.02.001. DOI
Renwick JAA, Hughes PR, Krull IS. Selective production of cis- and trans-verbenol from (–)-and (+)-α-pinene by a bark beetle. Science. 1976;191:199–201. doi: 10.1126/science.1246609. PubMed DOI
Rouault G, Candau J-N, Lieutier F, Nageleisen L-M, Martin J-C, Warzée N. Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe. Ann For Sci. 2006;63:613–624. doi: 10.1051/forest:2006044. DOI
Sambaraju KR, Carroll AL, Aukema BH. Multiyear weather anomalies associated with range shifts by the mountain pine beetle preceding large epidemics. For Ecol Manag. 2019;438:86–95. doi: 10.1016/j.foreco.2019.02.011. DOI
Sancho-Knapik D, Sanz MA, Peguero-Pina JJ, Niinemets U, Gil-Pelegrín E. Changes of secondary metabolites in Pinus sylvestris L needles under increasing soil water deficit. Ann For Sci. 2017 doi: 10.1007/s13595-017-0620-7. DOI
Santos AM, Vasconcelos T, Mateus E, Farrall MH, Gomes da Silva MD, Paiva MR, Branco M. Characterization of the volatile fraction emitted by phloems of four pinus species by solid-phase microextraction and gas chromatography-mass spectrometry. J Chromatogr A. 2006;1105:191–198. doi: 10.1016/j.chroma.2005.10.049. PubMed DOI
Schiebe C, Hammerbacher A, Birgersson G, et al. Inducibility of chemical defenses in Norway spruce bark is correlated with unsuccessful mass attacks by the spruce bark beetle. Oecologia. 2012;170:183–198. doi: 10.1007/s00442-012-2298-8). PubMed DOI
Schiebe C, Unelius CR, Ganji S, Binyameen M, Birgersson G, Schlyter F. Styrene, (+)-trans-(1R,4S,5S)-4-thujanol and oxygenated monoterpenes related to host stress elicit strong electrophysiological responses in the bark beetle Ips typographus. J Chem Ecol. 2019;45:474–489. doi: 10.1007/s10886-019-01070-8. PubMed DOI PMC
Schlyter F, Birgersson G. Forest Beetles. In: Hardie J, Minks AK, editors. Pheromones of non-lepidopteran insects associated with agricultural plants. England: CAB International; 1999. pp. 113–148.
Schlyter F, Löfqvist J. Response of walking spruce bark beetles Ips typographus to pheromone produced in different attack phases. Entomol Exp Appl. 1986;41:219–230. doi: 10.1111/j.1570-7458.1986.tb00532.x. DOI
Schlyter F, Birgersson G, Byers JA, Löfqvist J, Bergström G. Field response of spruce bark beetle, Ips typographus, to aggregation pheromone candidates. J Chem Ecol. 1987;13:701–716. doi: 10.1007/BF01020153. PubMed DOI
Schlyter F, Birgersson G, Leufvén A. Inhibition of attraction to aggregation pheromone by verbenone and ipsenol. J Chem Ecol. 1989;15:2263–2277. doi: 10.1007/BF01014114. PubMed DOI
Schönwitz R, Kloos M, Merk L, ZIegler H. Patterns of monoterpenes stored in the needles of Picea abies (L) Karst from several locations in mountainous regions of southern Germany. Trees. 1990;4:27–33. doi: 10.1007/BF00226237. DOI
Seidl R, Muller J, Hothorn T, Bassler C, Heurich M, Kautz M. Small beetle, large-scale drivers: how regional and landscape factors affect outbreaks of the European spruce bark beetle. J Appl Ecol. 2016;53:530–540. doi: 10.1111/1365-2664.12540. PubMed DOI PMC
Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 2014;37:153–161. doi: 10.1111/pce.12141. PubMed DOI PMC
Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B. Response of phenylpropanoidpPathway and the role of polyphenols in plants under abiotic stress. Molecules. 2019 doi: 10.3390/molecules24132452. PubMed DOI PMC
Silvestrini E, Michelozzi M, Skroppa T, Brancaleoni E, Ciccioli P. Characterisation of different clones of Picea abies (L.) Karst using head-space sampling of cortical tissues combined with enantioselective capillary gas chromatography for the separation of chiral and non-chiral monoterpenes. J Chromatogr A. 2004;1034:183–189. doi: 10.1016/j.chroma.2004.02.001. PubMed DOI
Six DL. Ecological and evolutionary determinants of bark beetle-fungus symbioses. Insects. 2012;3:339–366. doi: 10.3390/insects3010339. PubMed DOI PMC
Six DL. The bark beetle holobiont: why microbes matter. J Chem Ecol. 2013;39:989–1002. doi: 10.1007/s10886-013-0318-8. PubMed DOI
Six DL. A major symbiont shift supports a major niche shift in a clade of tree-killing bark beetles. Ecol Entomol. 2019;45:190–201. doi: 10.1111/een.12786. DOI
Six DL, Elser JJ. Mutualism is not restricted to tree-killing bark beetles and fungi: the ecological stoichiometry of secondary bark beetles, fungi, and a scavenger. Ecol Entomol. 2020 doi: 10.1111/een.12897. DOI
Six DL, Wingfield BD. The role of phytopathogenicity in bark beetle–fungus symbioses: a challenge to the classic paradigm. Annu Rev Entomol. 2011;56:255–272. doi: 10.1146/annurev-ento-120709-144839. PubMed DOI
Six DL, Vergobbi C, Cutter M. Are survivors different? Genetic-based selection of trees by mountain pine beetle during a climate change-driven outbreak in a high-elevation pine forest. Front Plant Sci. 2018;9:993. doi: 10.3389/fpls.2018.00993. PubMed DOI PMC
Solheim H. Oxygen deficiency and spruce resin inhibition of growth of blue-stain fungi associated with Ips typographus. Mycol Res. 1991;95:1387–1392. doi: 10.1016/S0953-7562(09)80390-0. DOI
Stadelmann G, Bugmann H, Wermelinger B, Bigler C. Spatial interactions between storm damage and subsequent infestations by the European spruce bark beetle. For Ecol Manag. 2014;318:167–174. doi: 10.1016/j.foreco.2014.01.022. DOI
Tan W, Blake TJ. Drought tolerance, abscisic acid and electrolyte leakage in fast-and slow-growing black spruce (Picea mariana) progenies. Physiol Plant. 2006;89:817–823. doi: 10.1111/j.1399-3054.1993.tb05290.x. DOI
Tausz M, Wonisch A, Peters J, Jiménez MS, Morales D, Grill D. Short-term changes in free radical scavengers and chloroplast pigments in Pinus canariensis needles as affected by mild drought stress. J Plant Physiol. 2001;158:213–219. doi: 10.1078/0176-1617-00178. DOI
Tausz M, Sircelj H, Grill D. The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J Exp Bot. 2004;55:1955–1962. doi: 10.1093/jxb/erh194. PubMed DOI
Telford A, Cavers S, Ennos RA, Cottrell JE. Can we protect forests by harnessing variation in resistance to pests and pathogens? Forestry. 2014;88:3–12. doi: 10.1093/forestry/cpu012. DOI
Tittiger C, Blomquist GJ. Pheromone biosynthesis in bark beetles. Curr Opin Insect Sci. 2017;24:68–74. doi: 10.1016/j.cois.2017.09.005. PubMed DOI
Tømmerås BÅ. Specialization of the olfactory receptor cells in the bark beetle Ips typographus and its predator Thanasimus formicarius to bark beetle pheromones and host tree volatiles. J Comp Physiol A. 1985;157:335–341. doi: 10.1007/BF00618123. DOI
Tømmerås BÅ, Mustaparta H. Enhanced attraction of Ips typographus by adding exo-brevicomin to pheromone traps. Naturwissenschaften. 1984;71:375–377. doi: 10.1007/BF00410747. DOI
Turcani M, Nakladal O. The results of manipulated experiments with inoculation of Ips typographus (L., 1758) to spruce trees under various levels of water stress. J For Sci. 2007;53:25–30. doi: 10.17221/2159-JFS. DOI
Turtola S, Manninen AM, Rikala R, Kainulainen PJ. Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce seedlings. J Chem Ecol. 2003;29:1982–1995. doi: 10.1023/A:1025674116183. PubMed DOI
Urbanek Krajnc A, Kristl J, Ivancic A. Application of salicylic acid induces antioxidant defense responses in the phloem of Picea abies and inhibits colonization by Ips typographus. For Ecol Manag. 2011;261:416–426. doi: 10.1016/j.foreco.2010.10.027. DOI
Urbanek Krajnc A, Novak M, Felicijan M, Kraševec N, Lešnik M, Zupanec N, Komel R. Antioxidative response patterns of Norway spruce bark to low-density Ceratocystis polonica inoculation. Trees. 2014;28:1145–1160. doi: 10.1007/s00468-014-1025-y. DOI
Viiri H, Annila E, Kitunen V, Niemelä P. Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica. Trees. 2001;15:112–122. doi: 10.1007/s004680000082. DOI
Wadke N, Kandasamy D, Vogel H, et al. The bark-beetle-associated fungus, Endoconidiophora polonica, utilizes the phenolic defense compounds of its host as a carbon source. Plant Physiol. 2016;171:914–931. doi: 10.1104/pp.15.01916. PubMed DOI PMC
Wallin KF, Raffa KF. Prior encounters modulate subsequent choices in host acceptance behavior by the bark beetle Ips pini. Entomol Exp Appl. 2002;103:205–218. doi: 10.1046/j.1570-7458.2002.00975.x. DOI
Wang Y, Lim L, Madilao L, Lah L, Bohlmann J, Breuil C. Gene discovery for enzymes involved in limonene modification or utilization by the mountain pine beetle-associated pathogen Grosmannia clavigera. Appl Environ Microb. 2014;80:4566–4576. doi: 10.1128/AEM.00670-14. PubMed DOI PMC
Wijerathna AN, Evenden ML. Energy use by the mountain pine beetle (Coleoptera: Curculionidae: Scolytinae) for dispersal by flight. Physiol Entomol. 2019;44:200–208. doi: 10.1111/phen.12290. DOI
Witzell J, Martín JA. Phenolic metabolites in the resistance of northern forest trees to pathogens—past experiences and future prospects. Can J For Res. 2008;38:2711–2727. doi: 10.1139/x08-112. DOI
Wood DL (1972) Selection and colonization of ponderosa pines by bark beetles. In: van Emden HF (ed) Insect/plant Relationships. Royal Entomological Society Symposium No. 6. Blackwell Scientific Publications Oxford, England, pp 101–107
Worrell R. Damage by the spruce bark beetle in south Norway 1970–80: A survey and factors affecting its occurrence. Medd fra Norsk Inst Skogforsk Rep Nor For Res Inst. 1983;38:1–34.
Yuvaraj JK, Roberts RE, Sonntag Y, et al. Putative ligand binding sites of two functionally characterized bark beetle odorant receptors. Biorxiv. 2020 doi: 10.1101/2020.03.07.980797. PubMed DOI PMC
Zeneli G, Krokene P, Christiansen E, Krekling T, Gershenzon J. Methyl jasmonate treatment of mature Norway spruce (Picea abies) trees increases the accumulation of terpenoid resin components and protects against infection by Ceratocystis polonica, a bark beetle-associated fungus. Tree Physiol. 2006;26:977–988. doi: 10.1093/treephys/26.8.977. PubMed DOI
Zhang Q-H, Schlyter F. Redundancy, synergism, and active inhibitory range of non-host volatiles in reducing pheromone attraction in European spruce bark beetle Ips typographus. Oikos. 2003;101:299–310. doi: 10.1034/j.1600-0706.2003.111595.x. DOI
Zhang Q-H, Schlyter F. Olfactory recognition and behavioural avoidance of angiosperm nonhost volatiles by conifer-inhabiting bark beetles. Agr For Entomol. 2004;6:1–19. doi: 10.1111/j.1461-9555.2004.00202.x. DOI
Zhao T, Krokene P, Björklund N, Långström B, Solheim H, Christiansen E, Borg-Karlson AK. The influence of Ceratocystis polonica inoculation and methyl jasmonate application on terpene chemistry of Norway spruce, Picea abies. Phytochem. 2010;71:1332–1341. doi: 10.1016/j.phytochem.2010.05.017. PubMed DOI
Zhao T, Borg-Karlson AK, Erbilgin N, Krokene P. Host resistance elicited by methyl jasmonate reduces emission of aggregation pheromones by the spruce bark beetle, Ips typographus. Oecologia. 2011;167:691–699. doi: 10.1007/s00442-011-2017-x. PubMed DOI
Zhao T, Krokene P, Hu J, et al. Induced terpene accumulation in Norway spruce inhibits bark beetle colonization in a dose-dependent manner. PLoS One. 2011;6:e26649. doi: 10.1371/journal.pone.0026649. PubMed DOI PMC
Zhao T, Axelsson K, Krokene P, Borg-Karlson AK. Fungal symbionts of the spruce bark beetle synthesize the beetle aggregation pheromone 2-methyl-3-buten-2-ol. J Chem Ecol. 2015;41:848–852. doi: 10.1007/s10886-015-0617-3. PubMed DOI
Zhao T, Ganji S, Schiebe C, et al. Convergent evolution of semiochemicals across kingdoms: bark beetles and their fungal symbionts. ISME J. 2019;13:1535–1545. doi: 10.1038/s41396-019-0370-7. PubMed DOI PMC
Zhao T, Kandasamy D, Krokene P, Chen J, Gershenzon J, Hammerbacher A. Fungal associates of the tree-killing bark beetle, Ips typographus, vary in virulence, ability to degrade conifer phenolics and influence bark beetle tunneling behavior. Fungal Ecol. 2019;38:71–79. doi: 10.1016/j.funeco.2018.06.003. DOI
Zinecker E (1957) Der große Fichtenborkenkäfer Ips typographus L. in seiner Abhängigkeit vom Standort - Site dependendy of the European spruce bark beetle Ips typographus Anz Schädlingsk 30: 99–104
Insight into the genomes of dominant yeast symbionts of European spruce bark beetle, Ips typographus