The spruce bark volatiles and internal phloem chemical profiles after the forest gap formation: the annual course

Authors

  • Veronika Šamajová Faculty of Ecology and Environmental Sciences, Technical University in Zvolen; Institute of Forest Ecology of the Slovak Academy of Sciences Author
  • Jana Marešová Institute of Forest Ecology of the Slovak Academy of Sciences Author
  • Andrej Majdák Institute of Forest Ecology of the Slovak Academy of Sciences Author
  • Rastislav Jakuš Institute of Forest Ecology of the Slovak Academy of Sciences Author
  • Miroslav Blaženec Institute of Forest Ecology of the Slovak Academy of Sciences Author

DOI:

https://doi.org/10.2478/foecol-2024-0016

Keywords:

forest edge, induced defense, Norway spruce, terpenes, tree predisposition

Abstract

Our study explores the impact of sudden gap formation on the bark volatile and internal chemical profiles of Norway spruce trees during the initial dry year of research plot 2018 following gap formation. We investigated the annual variation in two main physiological traits of Norway spruce trees at the forest edge (FE) and in the forest interior (FI): bark monoterpene (MT) emission spectra and internal phloem MT composition. Given that gap formation increases the solar radiation dose and temperature for trees at the forest edge, we hypothesized that the concentrations of airborne terpenes released from the tree bark and internal phloem terpenes will increase as a consequence of induced tree defenses. Our findings demonstrate significant increases in both airborne terpene concentrations and internal terpene composition in trees at the forest edge compared to the control trees in the forest interior. This study provides novel insights into the annual dynamics of bark monoterpenes following forest edge establishment and underscores the physiological changes experienced by trees in response to the gap formation.

References

Bäck, J., Aalto, J., Henrikkson, M., Hakola, H., He, Q., Boy, M., 2012. Chemodiversity of a Scots pine stand and implications for terpene air concentrations. Biogeo-sciences, 9: 689–702. https://doi.org/10.5194/bg-9-689-2012

Baier, P., Bader, R., Rosner, S., 1999. Monoterpene content and monoterpene emission of Norway spruce (Picea abies (L.) Karst.) bark in relation to primary attraction of bark beetles (Col. Scolytidae). In Physiology and genetics of tree-phytophage interactions: International symposium. Les Colloques /INRA, 90. Paris: INRA, p. 249–259.

Blomquist, G.J., Figueroa-Teran, R., Aw, M., Song, M., Gorzalski, A., Abbott, N.L., Chang, E., Tittiger, C., 2010. Pheromone production in bark beetles. Insect Biochemistry and Molecular Biology, 40: 699–712. https://doi.org/10.1016/j.ibmb.2010.07.013

Bufler, U., Seufert, G., Jüttner, F., 1990. Monoterpene patterns of different tissues and plant parts of Norway spruce (Picea abies L. Karst.). Environmental Pollution, 68 : 367–375. https://doi.org/10.1016/0269-7491(90)90038-e

Byers, J.A., Wood, D.L., 1981. Interspecific effects of pheromones on the attraction of the bark beetles, Dendroctonus brevicomis and Ips paraconfusus in the laboratory. Journal of Chemical Ecology, 7: 9–18. https://doi.org/10.1007/bf00988631

Celedon, J.M., Bohlmann, J., 2019. Oleoresin defenses in conifers: chemical diversity, terpene synthases and limitations of oleoresin defense under climate change. New Phytologist, 224: 1444–1463. https://doi.org/10.1111/nph.15984

Celedon, J.M., WhitehilL, J.G.A., Madilao, L.L., Bohl mann, J., 2020. Gymnosperm glandular trichomes: expanded dimensions of the conifer terpenoid defense system. Scientific Reports, 10: 12464. https://doi.org/10.1038/s41598-020-69373-5

Duan, Q., Bonn, B., Kreuzwieser, J., 2020. Terpenoids are transported in the xylem sap of Norway spruce. Plant, Cell & Environment, 43: 1766–1778. https://doi.org/10.1111/pce.13763

Franceschi, V.R., Krokene, P., Christiansen, E., Krekling, T., 2005. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytolo-gist, 167: 353–376. https://doi.org/10.1111/j.1469-8137.2005.01436.x

Ghimire, B., Wiliams, C.A., Collatz, G.J., Vanderhoof, M., Rogan, J., Kulakowski, D., Masek, J.G., 2015. Large carbon release legacy from bark beetle outbreaks across Western United States. Global Change Biology, 21: 3087–3101. https://doi.org/10.1111/gcb.12933

Ghirardo, A., Koch, K., Taipale, R., Zimmer, I., Sschnitzler, J.-P., Rinne, J., 2010. Determination of de novo and pool emissions of terpenes from four common boreal/alpine trees by 13CO2 labelling and PTR-MS. Plant, Cell & Environment, 33: 781–792. https://doi.org/10.1111/j.1365-3040.2009.02104.x

Gitau, C.W., Bashford, R., Carnegie, A.J., Gurr, G.M., 2013. A review of semiochemicals associated with bark beetle (Coleoptera: Curculionidae: Scolytinae) pests of coniferous trees: a focus on beetle interactions with other pests and their associates. Forest Ecology and Management, 297: 1–14. https://doi.org/10.1016/j.foreco.2013.02.019

Gramber, W., Kreuzwieser, J., Wisthaler, A., Cojocariu, C., Graus, M., Rennenber, H., Steiger, D., Steinbrecher, R., Hansel, A., 2006. VOC emissions from Norway spruce (Picea abies L. [Karst]) twigs in the field—Results of a dynamic enclosure study. Atmospheric Environment, 40, Suppl. 1: 128–137. https://doi.org/10.1016/j.atmosenv.2006.03.043

Hlásny, T., Zimová, S., Merganičová, K., Štepánek P., Modlinger, R., Turčáni, M., 2021. Devastating outbreak of bark beetles in the Czech Republic: drivers, impacts, and management implications. Forest Ecology and Management, 490: 119075. https://doi.org/10.1016/j.foreco.2021.119075

Holopainen, J.K., Virjamo, V., Ghimire, R.P., Blande, J.D., Julkunen-Tiitto, R., Kivimäenpää, M., 2018. Climate Effects on Secondary Compounds of Forest Trees in the Northern Hemisphere. Frontiers in Plant Science, 9: 1445. https://doi.org/10.3389/fpls.2018.01445

Huang, J., Hammerbacher, A., Weinhold, A., Reichelt, M., Gleixner, G., Behrendt, T., Van Damm, N.M., Sala, A., Gershenzon, J., TrumborE, S., Hartmann, H., 2018. Eyes on the future – evidence for trade-offs between growth, storage and defense in Norway spruce. New Phytologist, 222: 144–158. https://doi.org/10.1111/nph.15522

Jakuš, R., Edwards-Jonášová, M., Cudlín, P., Blaženec, M., Ježík, M., Havlíček, F., Moravec, I., 2011a. Characteristics of Norway spruce trees (Picea abies) surviving a spruce bark beetle (Ips typographus L.) outbreak. Trees, 25: 965–973 (2011). https://doi.org/10.1007/s00468-011-0571-9

Jakuš, R., Grodzki, W., Ježík, M., Jachym, M., 2003. Definition of spatial patterns of bark beetle Ips typographus (L) outbreak spreading in Tatra Mountains (Central Europe) using GIS. In McManus, M.L., Liebhold, A.M. (eds). Proceedings: ecology survey and management of forest insects. General Technical Report NE, 311. USDA Forest Service, Northeastern Research Station, p. 25–32.

Jakuš, R., Zajíčkova, L., Cudlín, P., Blaženec, M., Turčani, M., Ježík, M., Lieutier, F., Schlyter, F., 2011b. Landscape-scale Ips typographus attack dynamics: from monitoring plots to GIS-based disturbance models. iForest - Biogeosciences and Forestry, 4: 256–261. https://doi.org/10.3832/ifor0589-004

Janson, R.W., 1993. Monoterpene emissions from Scots pine and Norwegian spruce. Journal of GeophysicalRe-search: Atmospheres, 98: 2839–2850. https://doi.org/10.1029/92jd02394

Jirošová, A., Kalinová, B., Modlinger, R., Jakuš, R., Unelius, C.R., Blaženec, M., Schlyter, F., 2022. Anti-attractant activity of (+)-trans-4-thujanol for Eurasian spruce bark beetle Ips typographus: novel potency for females. Pest Management Science, 78: 1992–1999. https://doi.org/10.1002/ps.6819

Juráň, S., Pallozzi, E., Guidolotti, G., Fares, S., Šigut, L., Calfapietra, C., Alivernini, A., Savi, F., Večeřová, K., Křumal, K., Večeřa, Z., Urban, O., 2017. Fluxes of biogenic volatile organic compounds above temperate Norway spruce forest of the Czech Republic. Agricultural and Forest Meteorology, 232: 500–513. https://doi.org/10.1016/j.agrformet.2016.10.005

Kautz, M., Schopf, R., Ohser, J., 2013. The “sun-effect”: microclimatic alterations predispose forest edges to bark beetle infestations. European Journal of Forest Research, 132: 453–465. https://doi.org/10.1007/s10342-013-0685-2

Kempf, K., Allwine, E., Westberg, H., Claiborn, C., Lamb, B., 1996. Hydrocarbon emissions from spruce species using environmental chamber and branch enclosure methods. Atmospheric Environment, 30: 1381–1389. https://doi.org/10.1016/1352-2310(95)00462-9

Kleist, E., Mentel, T.F., Andres, S., Bohne, A., Folkers, A., Kiendler-Scharr, A., Rudich, Y., Springer, M., Tillmann, R., Wildt, J., 2012. Irreversible impacts of heat on the emissions of monoterpenes, sesquiterpenes, phenolic BVOC and green leaf volatiles from several tree species. Biogeosciences, 9: 5111–5123. https://doi.org/10.5194/bg-9-5111-2012

Klimetzek, D., Francke, W., 1980. Relationship between the enantiomeric composition of α-pinene in host trees and the production of verbenols in Ips species. Experientia, 36: 1343–1345. https://doi.org/10.1007/BF01960087

Lapin, M., Faako, P., Melo, M., Stastny, P., Tomlain, J., 2002. Climatic regions, 1: 1 000000. In Atlas krajiny Slovenskej republiky. Landscape atlas of the Slovak Republic. Bratislava: Ministerstvo životného prostredia SR; Banská Bystrica: Slovenská agentúra životného prostredia, p. IV, 95.

Madmony, A., Tognetti, R., Zamponi, L., Cappreti, P., Michelozzi, M., 2018. Monoterpene responses to interacting effects of drought stress and infection by the fungus Heterobasidion parviporum in two clones of Norway spruce (Picea abies). Environmental and Experimental Botany, 152: 137–148. https://doi.org/10.1016/j.envexpbot.2018.03.007

Majdák, A., Jakuš, R., Blaženec, M., 2021. Determination of differences in temperature regimes on healthy and bark-beetle colonised spruce trees using a handheld thermal camera. iForest - Biogeosciences and Forestry, 14: 203–211. https://doi.org/10.3832/ifor3531-014

Marchese, J.A., Ferreira, J.F.S., Rehder, V.L.G., Rodrigues, O., 2010. Water deficit effect on the accumulation of biomass and artemisinin in annual wormwood (Artemisia annua L., Asteraceae). Brazilian Journal of Plant Physiology, 22: 1–9. https://doi.org/10.1590/s1677-04202010000100001

Marešová, J., Majdák, A., Jakuš, R., Hradecký, J., Kali-nová, B., Blaženec, M., 2020. The short-term effect of sudden gap creation on tree temperature and volatile composition profiles in a Norway spruce stand. Trees, 34: 1397–1409. https://doi.org/10.1007/s00468-020-02010-w

Mezei, P., Jakuš, R., Blaženec, M., Belánová, S., Šmídt, J., 2011. Population dynamics of spruce bark beetle in a nature reserve in relation to stand edges conditions. Folia Oecologica, 38: 73–79.

Mezei, P., Potterf, M., Škvarenina, J., Rasmussen, J.G., Jakuš, R., 2019. Potential solar radiation as a driver for bark beetle infestation on a landscape scale. Forests, 10: 604. https://doi.org/10.3390/f10070604

Moukhtar, S., Couret, C., Rouil, L., Simon, V., 2006. Biogenic Volatile Organic Compounds (BVOCs) emissions from Abies alba in a French forest. Science of The Total Environment, 354: 232–245. https://doi.org/10.1016/j.scitotenv.2005.01.044

Netherer, S., Hammerbacher, A., 2022. The Eurasian spruce bark beetle in a warming climate: phenology, behavior, and biotic interactions. In Bark beetle management, ecology, and climate change. London: Academic Press, p. 89–131. https://doi.org/10.1016/b978-0-12-822145-7.00011-8

Netherer, S., Kandasamy, D., Jirošová, A., Kalinová, B., Schebeck, M., Schlyter, F., 2021. Interactions among Norway spruce, the bark beetle Ips typographus and its fungal symbionts in times of drought. Journal of Pest Science, 94: 591–614. https://doi.org/10.1007/s10340-021-01341-y

Niinemets, Ü., 2015. Uncovering the hidden facets of drought stress: secondary metabolites make the difference. Tree Physiology, 36: 129-132. https://doi.org/10.1093/treephys/tpv128

Niinemets, Ü., 2010. Mild versus severe stress and BVOCs: thresholds, priming and consequences. Trends in Plant Science, 15: 145–153. https://doi.org/10.1016/j.tplants.2009.11.008

Nybakken, L., Floistad, I.S., Mageroy, M., Lomsdal, M., Stralberg, S., Krokene, P., Asplund, J., 2021. Constitutive and inducible chemical defences in nursery-grown and naturally regenerated Norway spruce (Picea abies) plants. Forest Ecology and Management, 491: 119180. https://doi.org/10.1016/j.foreco.2021.119180

Persson, Y., Schurgers, G., Ekberg, A., Holst, T., 2016. Effects of intra-genotypic variation, variance with height and time of season on BVOC emissions. Meteorologische Zeitschrift, 25: 377–388. https://doi.org/10.1127/metz/2016/0674

Phillips, M.A., Croteau, R.B., 1999. Resin-based defenses in conifers. Trends in Plant Science, 4: 184–190. https://doi.org/10.1016/S1360-1385(99)01401-6

Raber, A.G., Peachey-Stoner, R.J., Cessna, S.G., Sider-hurst, M.S., 2021. Headspace GC-MS analysis of differences in intra- and interspecific Terpene profiles of Picea pungens Engelm. and P. abies (L.) Karst. Phytochemistry, 181: 112541. https://doi.org/10.1016/j.phytochem.2020.112541

Raffa, K.F., Powell, E.N., Towsend, P.A., 2013. Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses. Proceedings of the National Academy of Sciences, 110: 2193–2198. https://doi.org/10.1073/pnas.1216666110

Rasmann, S., Chassin, E., Bilat, J., Glauser G., Reymond, P., 2015. Trade-off between constitutive and inducible resistance against herbivores is only partially explained by gene expression and glucosinolate production. Journal of Experimental Botany, 66: 2527–2534. https://doi.org/10.1093/jxb/erv033

Schiebe, C., Hammerbacher, A., Birgersson, G., Witzell, J., Brodelius, P.E., Gershenzon, J., Hansson, B.S., Krokene, P., Schlyter, F., 2012a. Inducibility of chemical defenses in Norway spruce bark is correlated with unsuccessful mass attacks by the spruce bark beetle. Oecologia, 170: 183–198. https://doi.org/10.1007/s00442-012-2298-8

Schiebe, C., 2012b. Attraction and resistance in the Picea abies – Ips typographus System. PhD thesis. Swedish University of Agricultural Sciences, Alnarp. 57 p. https://doi.org/10.13140/2.1.1229.1363

Schönwitz, R., Lohwasser, K., Kloos, M., Ziegler, H., 1990. Seasonal variation in the monoterpenes in needles of Picea abies (L.) Karst. Trees, 4: 34–40. https://doi.org/10.1007/bf00226238

Schütte, H.-R., 1984. Secondary plant substances. Monoterpenes. In Esser, K., Kubitzki, K., Runge, M., Schnepf, E., Ziegler, H. (eds). Progress in Botany / Fortschritte der Botanik: Morphology - Physiology - Genetics Taxonomy - Geobotany / Morphologie - Physiologie - Genetik Systematik - Geobotanik. Berlin, Heidelberg: Springer, p. 119–139. https://doi.org/10.1007/978-3-642-69985-6_9

Seybold, S.J., Huber, D.P.W., Lee, J.C., Graves, A.D., Bohlmann, J., 2006. Pine monoterpenes and pine bark beetles: a marriage of convenience for defense and chemical communication. Phytochemistry Reviews, 5: 143–178. https://doi.org/10.1007/s11101-006-9002-8

Sousa, M., Birgersson, G., Karlsson Green, K., Pollet, M., Becher, P.G., 2023. Odors attracting the long-legged predator Medetera signaticornis Loew to Ips typographus L. infested Norway spruce trees. Journal of Chemical Ecology, 49: 451–464. https://doi.org/10.1007/s10886-023-01405-6

Steinbecher, R., Ziegler, H., Eichstädter, G., Fehsenfeld, U., Gabriel, R., Kolb, Ch., Rabong, R., Schönwitz, R., Schürmann, W., 1997. Monoterpene and isoprene emission in Norway spruce forests. In Biosphere-atmosphere exchange of pollutants and trace substances. Vol. 4. Berlin, Heidelberg: Springer, p. 352–365. https://doi.org/10.1007/978-3-662-03394-4_27

Stříbrská, B., Hradecký, J., Čepl, J., Tomášková, I., Jakuš, R., Modlinger, R., Netherer, S., Jirošová, A., 2022. Forest margins provide favourable microclimatic niches to swarming bark beetles, but Norway spruce trees were not attacked by Ips typographus shortly after edge creation in a field experiment. Forest Ecology and Management, 506: 119950. https://doi.org/10.1016/j.foreco.2021.119950

Szabó, K., Radácsi, P., rajhárt, P., Ladányi, M., Németh, É., 2017. Stress-induced changes of growth, yield and bio-active compounds in lemon balm cultivars. Plant Physiology and Biochemistry, 119: 170–177. https://doi.org/10.1016/j.plaphy.2017.07.019

Turtola, S., Manninen, A.-M., Rikala, R., Kainulainen, P., 2003. Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce Seedlings. Journal of Chemical Ecology, 29: 1981–1995. https://doi.org/10.1023/A:1025674116183

Van Meeningen, Y., Wang, M., Karlsson, T., Seifert, A., Schurgers, G., Rinnan, R., Holst, T., 2017. Isoprenoid emission variation of Norway spruce across a European latitudinal transect. Atmospheric Environment, 170: 45–57. https://doi.org/10.1016/j.atmosenv.2017.09.045

Von Rudollf, E., 1975. Volatile leaf oil analysis in chemo-systematic studies of North American conifers. Bio-chemical Systematics and Ecology, 2: 131–167. https://doi.org/10.1016/0305-1978(75)90055-1

Yassaa, N., Song, W., Lelieveld, J., Vanhatalo, A., Bäck, J., Williams, J., 2012. Diel cycles of isoprenoids in the emissions of Norway spruce, four Scots pine chemo-types, and in Boreal forest ambient air during Humppa-Copec-2010. Atmospheric Chemistry and Physics, 12: 7215–7229. https://doi.org/10.5194/acp-12-7215-2012

Yuvaraj, J.K., Roberts, R.E., Sonntag, Y., Hou, X.-Q., Grosse-wilde, E., Machara, A., Zhang, D.-D., Hans-son, B.S., Johanson, U., Löfstedt, C., Andersson, M.N., 2021. Putative ligand binding sites of two functionally characterized bark beetle odorant receptors. BMC Biology, 19: article no. 16. https://doi.org/10.1186/s12915-020-00946-6

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

Zulak, K.G., Lippert, D.N., Kuzyk, M.A., Domanski, D., Chou, T., Borchers, C.H., Bohlmann, J., 2009. Targeted proteomics using selected reaction monitoring reveals the induction of specific terpene synthases in a multi-level study of methyl jasmonate-treated Norway spruce (Picea abies). The Plant Journal, 60: 1015–1030. https://doi.org/10.1111/j.1365-313X.2009.04020

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2024-07-29

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