Bark beetles kill apparently vigorous conifers during epidemics by means of pheromone-mediated aggregation. During non-endemic conditions the beetles are limited to use trees with poor defense, like wind-thrown. To find olfactory cues that help beetles to distinguish between trees with strong or weak defense, we collected volatiles from the bark surface of healthy felled or standing Picea abies trees. Furthermore, living trees were treated with methyl jasmonate in order to induce defense responses. Volatiles were analyzed by combined gas chromatography and electroantennographic detection (GC-EAD) on Ips typographus antennae. Compounds eliciting antennal responses were characterized by single sensillum recording for identification of specific olfactory sensory neurons (OSN). Release of monoterpene hydrocarbons decreased, while oxygenated compounds increased, from spring to early summer in felled trees. In both beetle sexes particular strong EAD activity was elicited by trace amounts of terpene alcohols and ketones. 4-Thujanol gave a very strong response and the absolute configuration of the tested natural product was assigned to be (+)-trans-(1R,4S,5S)-thujanol by stereoselective synthesis and enantioselective gas chromatography. One type of OSN responded to all ketones and five other OSN were characterized by the type of compounds that elicited responses. Three new OSN classes were found. Of the eight EAD-active compounds found in methyl jasmonate-treated bark, the known anti-attractant 1,8-cineole was the one most strongly induced. Our data support the hypothesis that highly active oxygenated host volatiles could serve as positive or negative cues for host selection in I. typographus and in other bark beetles.

Chemical Ecology Department Plant Protection Biology Swedish University of Agricultural Sciences PO Box 102 230 53 Alnarp Sweden

Department Chemistry and Biomedical Sciences Linnaeus University Stuvaregatan 2 392 31 Kalmar Sweden

Department of Entomology Faculty of Agricultural Sciences and Technology Bahauddin Zakariya University Multan 60800 Pakistan

Faculty of Forestry and Wood Sci Excellent Team for Mitigation Czech University Life Sci Prague Kamycka 129 Prague 6 16521 Suchdol Czech Republic

Zobrazit více v PubMed

Anderbrant O, Schlyter F, Birgersson G. Intraspecific competition affecting parents and offspring in the bark beetle Ips typographus. Oikos. 1985;45:89–98. doi: 10.2307/3565226. DOI

Andersson MN (2012) Mechanisms of odor coding in coniferous bark beetles: from neuron to behavior and application. Psyche (Camb Mass) 2012:Article ID 149572 10.1155/2012/149572

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, Jakus R, Zhang Q-H, 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, Binyameen M, Schlyter F. Attraction modulated by spacing of pheromone components and anti-attractants in a bark beetle and a moth: a smaller scale of action in the moth. J Chem Ecol. 2011;37:899–911. doi: 10.1007/s10886-011-9995-3. PubMed DOI

Andersson MN, Schlyter F, Hill SR, Dekker T. What reaches the antenna? How to calibrate odor flux and ligand-receptor affinities. Chem Senses. 2012;37:403–420. doi: 10.1093/chemse/bjs009. PubMed DOI

Azeem M, Rajarao GK, Nordenhem H, Nordlander G, Borg-Karlson AK. Penicillium expansum volatiles reduce pine weevil attraction to host plants. J Chem Ecol. 2013;39:120–128. doi: 10.1007/s10886-012-0232-5. PubMed DOI PMC

Baeckstrom P, Koutek B, Saman D, Vrkoc J. A convenient synthesis of trans-Sabinene hydrate from (−)-3-thujol via a highly selective ene reaction of singlet oxygen. Bioorgan Med Chem. 1996;4:419–421. doi: 10.1016/0968-0896(96)00020-X. PubMed DOI

Baier P, Bader R. Gehalt und Emission von Monoterpenen der Fichtenrinde und deren Bedeutung für die Primärattraktion von Borkenkäfern (Coleoptera, Scolytidae) Mitt Dtsch Ges Allg Angew Entomol. 1997;11:639–643.

Bakke A, Frøyen P, Skattebøl L. Field response to a new pheromonal compound isolated from Ips typographus. Naturwissenschaften. 1977;64:98–99. doi: 10.1007/BF00437364. DOI

Binyameen M, Jankuvova J, Blazenec M, Jakus R, Song L, Schlyter F, Andersson MN. Co-localisation 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. 2016;73:247–256. doi: 10.1007/s13595-015-0494-5. DOI

Boone CK, Aukema BH, Bohlmann J, Carroll AL, Raffa KF. Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species. Can J For Res. 2011;41:1174–1188. doi: 10.1139/x11-041. DOI

Byers JA. An encounter rate model of bark beetle populations searching at random for susceptible host trees. Ecol Model. 1996;91:57–66. doi: 10.1016/0304-3800(95)00166-2. DOI

Byers JA, Lanne BS, Löfqvist J. Host tree unsuitability recognized by pine shoot beetles in flight. Experientia. 1989;45:489–492. doi: 10.1007/BF01952042. DOI

de Fouchier A, Walker WB, Montagné N, Steiner C, Binyameen M, Schlyter F, Chertemps T, Maria A, François MC, Monsempes C, Anderson P, Hansson BS, Larsson MC, Jacquin-Joly E. Functional evolution of Lepidoptera olfactory receptors revealed by deorphanization of a moth repertoire. Nature Comm. 2017;8:15709. doi: 10.1038/ncomms15709. PubMed DOI PMC

El-Sayed A (2018) The Pherobase: database of insect pheromones and semiochemicals. www.pherobase.com. Accessed 28 Oct 2018

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, Kamme T, Christiansen E. A host monoterpene influences Ips typographus (Coleoptera : Curculionidae, Scolytinae) responses to its aggregation pheromone. Agric For Entomol. 2007;9:135–140. doi: 10.1111/j.1461-9563.2007.00329.x. DOI

Faccoli M, Schlyter F. Conifer phenolic resistance markers are bark beetle antifeedant semiochemicals. Agric For Entomol. 2007;9:237–245. doi: 10.1111/j.1461-9563.2007.00339.x. 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

Gries G, Nolte R, Sanders W. Computer simulated host selection in Ips typographus. Entomol Exp Appl. 1989;53:211–217. doi: 10.1111/j.1570-7458.1989.tb03568.x. DOI

Gries G, Smirle MJ, Leufvén A, Miller DR, Borden JH, Whitney HS. Conversion of phenylalanine to toluene and 2-phenylethanol by the pine engraver Ips pini (say) (Coleoptera, Scolytidae) Cell Mol Life Sci. 1990;46:329–331. doi: 10.1007/BF01951781. DOI

Hayes JL, Strom BL. 4-Allylanisole as an inhibitor of bark beetle (Coleoptera: Scolytidae) aggregation. J Econ Entomol. 1994;87:1586–1594. doi: 10.1093/jee/87.6.1586. DOI

Hulcr J, Ubik K, Vrkoc J. The role of semiochemicals in tritrophic interactions between the spruce bark beetle Ips typographus, its predators and infested spruce. J Appl Entomol. 2006;130:275–283. doi: 10.1111/j.1439-0418.2006.01069.x. DOI

Hunt DWA, Borden JH, Lindgren BS, Gries G. The role of autoxidation of α-pinene in the production of pheromones of Dendroctonus ponderosae (Coleoptera: Scolytidae) Can J For Res. 1989;19:1275–1282. doi: 10.1139/x89-194. DOI

Jakus R, Blazenec M. Influence of the proportion of (−)-α-pinene in pheromone bait on Ips typographus (Col., Scolytidae) catch in pheromone trap barriers and in single traps. J Appl Entomol. 2003;127:91–95. doi: 10.1046/j.1439-0418.2003.00695.x. DOI

Krokene P, Nagy NE, Solheim H. Methyl jasmonate and oxalic acid treatment of Norway spruce: anatomically based defense responses and increased resistance against fungal infection. Tree Physiol. 2008;28:29–35. doi: 10.1093/treephys/28.1.29. PubMed DOI

Larkov O, Dunkelblum E, Zada A, Lewinsohn E, Freiman L, Dudai N, Ravid U. Enantiomeric composition of (E)- and (Z)-sabinene hydrate and their acetates in five Origanum spp. Flavour Fragr J. 2005;20:109–114. doi: 10.1002/ffj.1386. DOI

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

Lindmark-Henriksson M, Isaksson D, Vaněk T, Valterová I, Högberg H-E, Sjödin K. Transformation of terpenes using a Picea abies suspension culture. J Biotechnol. 2004;107:173–184. doi: 10.1016/j.jbiotec.2003.10.009. PubMed DOI

Marriott P, Shellie R, Cornwell C. Gas chromatographic technologies for the analysis of essential oils. J Chromatogr A. 2001;936:1–22. doi: 10.1016/S0021-9673(01)01314-0. PubMed DOI

Martin DM, 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;129:1003–1018. 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

Mulock P, Christiansen E. The threshold of successful attack by Ips typographus on Picea abies: a field experiment. For Ecol Manag. 1986;14:125–132. doi: 10.1016/0378-1127(86)90097-6. DOI

Pettersson EM, Boland W. Potential parasitoid attractants, volatile composition throughout a bark beetle attack. Chemoecology. 2003;13:27–37. doi: 10.1007/s000490300003. DOI

Raffa KF, Berryman A. Physiological differences between lodgepole pines resistant and susceptible to the mountain pine beetle and associated microorganisms. Environ Entomol. 1982;11:486–492. doi: 10.1093/ee/11.2.486. DOI

Raffa KF, Berryman AA. Accumulation of monoterpenes and associated volatiles following inoculation of grand fir with a fungus transmitted by the fir engraver, Scolytus ventralis (Coleoptera: Scolytidae) Can Entomol. 1982;114:797–810. doi: 10.4039/Ent114797-9. DOI

Raffa KF, Berryman AA. Interacting selective pressures in conifer-bark beetle systems: a basis for reciprocal adaptations? Am Nat. 1987;129:234–262. doi: 10.1086/284633. DOI

Raffa KF, Smalley EB. Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle-fungal complexes. Oecologia. 1995;102:285–295. doi: 10.1007/BF00329795. PubMed DOI

Raffa KF, Andersson MN, Schlyter F (2016) Host selection by bark beetles: playing the odds in a high-stakes game. In: Blomquist G, Tittinger C (eds) Advances in insect physiology, vol 50. Elsevier Ltd, pp 1–74. 10.1016/bs.aiip.2016.02.001

Schiebe C, Blaženec M, Jakuš R, Unelius CR, Schlyter F. Semiochemical diversity diverts bark beetle attacks from Norway spruce edges. J Appl Entomol. 2011;135:726–737. doi: 10.1111/j.1439-0418.2011.01624.x. DOI

Schiebe C, Hammerbacher A, Birgersson G, Witzell J, Brodelius PE, Gershenzon J, Hansson BS, Krokene P, Schlyter F. 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

Schlyter F, Birgersson G (1999) Forest beetles. In: Hardie J, Minks AK (eds) Pheromones in non-lepidopteran insects associated with agricultural plants. CAB International, pp 113–148 ISBN 9780851993454

Schlyter F, Cederholm I. Separation of the sexes of living spruce bark beetles, Ips typographus (L.), (Coleoptera: Scolytidae) Z Ang Entomol. 1981;92:42–47. doi: 10.1111/j.1439-0418.1981.tb01650.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, Leufven A. Inhibition of attraction to aggregation pheromone by verbenone and ipsenol. Density regulation mechanisms in bark beetle Ips typographus. J Chem Ecol. 1989;15:2263–2277. doi: 10.1007/BF01014114. PubMed DOI

Tømmerås BA, Mustaparta H. Chemoreception of host volatiles in the bark beetle Ips typographus. J Comp Physiol. 1987;161:705–710. doi: 10.1007/BF00605011. DOI

Tunset K, Nilssen AC, Andersen J. Primary attraction in host recognition of coniferous bark beetles and bark weevils (Col., Scolytidae and Curculionidae) J Appl Entomol. 1993;115:155–169. doi: 10.1111/j.1439-0418.1993.tb00375.x. DOI

Unelius CR, Schiebe C, Bohman B, Andersson MN, Schlyter F. Non-host volatile blend optimization for forest protection against the European spruce bark beetle, Ips typographus. PLoS One. 2014;9:e85381. doi: 10.1371/journal.pone.0085381. PubMed DOI PMC

van den Dool H, Kratz PD. A generalization of the retention index system including linear temperature programmed gas—liquid partition chromatograph. J Chromatogr A. 1963;11:463–471. doi: 10.1016/S0021-9673(01)80947-X. 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 non-host volatiles by conifer bark beetles. Agric For Entomol. 2004;6:1–19. doi: 10.1111/j.1461-9555.2004.00202.x. DOI

Zhang Q-H, Birgersson G, Zhu J, Löfstedt C, Löfqvist J, Schlyter F. Leaf volatiles from nonhost deciduous trees: variation by tree species, season and temperature, and electrophysiological activity in Ips typographus. J Chem Ecol. 1999;25:1923–1943. doi: 10.1023/A:1020994119019. DOI

Zhao T, Krokene P, Björklund N, Långström B, Solheim H, Christiansen E, Borg-Karlson A-K. The influence of Ceratocystis polonica inoculation and methyl jasmonate application on terpene chemistry of Norway spruce, Picea abies. Phytochemistry. 2010;71:1332–1341. doi: 10.1016/j.phytochem.2010.05.017. PubMed DOI

Zhao T, Krokene P, Hu J, Christiansen E, Björklund N, Långström B, Solheim H, Borg-Karlson AK. 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

Interactions among Norway spruce, the bark beetle Ips typographus and its fungal symbionts in times of drought

Putative ligand binding sites of two functionally characterized bark beetle odorant receptors