1 Introduction
6.5 CONCLUSIONS AND IMPLICATIONS
This study showed that herbivore damage to Scots pine shoots and Norway spruce tree trunks triggers BVOC emissions, but that herbivore feeding on foliage of Scots pine seedlings may reduce below-ground BVOC emissions. Herbivory and climate change relevant abiotic factors, separately and in combination, altered the emission rates of BVOCs from Scots pine shoots.
Effects of herbivore-feeding stress on localized shoot VOC emissions of Scots pine were reduced by warming, but enhanced upon exposure to elevated ozone in combination with elevated temperature. Herbivore-induced systemic monoterpene emissions were increased by elevated ozone during feeding damage, and enhanced by application of elevated nitrogen nearly three months after the start of feeding.
These results are good examples for showing how complicated the effects of simultaneous plant stress factors on BVOC emissions could be.
It can be concluded that there is great potential for further increases in BVOC emissions from boreal conifer forests with
expected future increases in insect outbreaks, warming, ozone concentrations and nitrogen availability in northern Europe. The results of this study are relevant for understanding the implications of a rapidly changing climate triggered by anthropogenic activity in northern boreal ecosystems. The predicted increases in biogenic VOC emissions may affect atmospheric chemistry and influence the global climate e.g.
through the formation of biogenic secondary organic aerosols and increases in concentrations of cloud condensation nuclei in the atmosphere. In long-term, this may have widespread impacts on biological systems of the Earth.
REFERENCES
Achotegui-Castells A, Llusia J, Hódar JA, Peñuelas J (2013) Needle terpene concentrations and emissions of two coexisting subspecies of Scots pine attacked by the pine processionary moth (Thaumetopoea pityocampa). Acta Physiologiae Plantarum 35: 3047–3058.
Ainsworth EA, Yendrek CR, Sitch S, Collins WJ, Emberson LD (2012) The effects of tropospheric ozone on net primary productivity and implications for climate change. Annual Review of Plant Biology 63: 637–661.
Allison SD, Treseder KK (2008) Warming and drying suppress microbial activity and carbon cycling in boreal forest soils.
Global Change Biology 14: 2898–2909.
Amin HS, Atkins PT, Russo RS, Brown AW, Sive B, Hallar AG, Huff Hartz KE (2012) Effect of bark beetle infestation on secondary organic aerosol precursor emissions.
Environmental Science and Technology 46: 5696–5703.
Amin HS, Russo RS, Sive B, Hoebeke ER, Dodson C, McCubbin IB, Hallar AG, Huff Hartz KE (2013) Monoterpene emissions from bark beetle infested Engelmann spruce trees. Atmospheric Environment 72: 130–133.
Arimura GI, Ozawa R, Maffei ME (2011) Recent advances in plant early signalling in response to herbivory.
International Journal of Molecular Sciences 12: 3723–3739.
Atkinson R, Arey J (2003) Gas-phase tropospheric chemistry of biogenic volatile organic compounds: a review.
Atmospheric Environment 37: 197–219.
Bäck J, Aalto J, Henriksson M, Hakola H, He Q, Boy M (2012) Chemodiversity of a Scots pine stand and implications for terpene air concentrations. Biogeosciences 9: 689–702.
Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects
of rising temperature on insect herbivores. Global Change Biology 8: 1–16.
Bengtsson A, Nilsson C (2007) Extreme value modelling of storm damage in Swedish forests. Natural Hazards and Earth System Sciences 7: 515–521.
Berggren Å, Björkman C, Bylund H, Ayres MP (2009) The distribution and abundance of animal populations in a climate of uncertainty. Oikos 118: 1121–1126.
Björkman C, Bylund H, Klapwijk MJ, Kollberg I, Schroeder M (2011) Insect pests in future forests: more severe problems?
Forests 2: 474–485.
Blanch JS, Peñuelas J, Llusià J (2007) Sensitivity of terpene emissions to drought and fertilization in terpene-storing Pinus halepensis and non-storing Quercus ilex. Physiologia Plantarum 131: 211–225.
Blanch JS, Peñuelas J, Sardans J, Llusià J (2009) Drought, warming and soil fertilization effects on leaf volatile terpene concentrations in Pinus halepensis and Quercus ilex.
Acta Physiologiae Plantarum 31: 207–218.
Blande JD, Tiiva P, Oksanen E, Holopainen JK (2007) Emission of herbivore-induced volatile terpenoids from two hybrids aspen (Populus tremula×tremuloides) clones under ambient and elevated ozone concentrations in the field. Global Change Biology 13: 2538–2550.
Blande JD, Turunen K, Holopainen JK (2009) Pine weevil feeding on Norway spruce bark has a stronger impact on needle VOC emissions than enhanced ultraviolet-B radiation. Environmental Pollution 157: 174–180.
Boucher O, Randall D, Artaxo P, Bretherton C, Feingold G, Forster P, Kerminen VM, Kondo Y, Liao H, Lohmann U, Rasch P, Satheesh SK, Sherwood S, Stevens B, Zhang XY (2013) Clouds and Aerosols Supplementary Material. In:
Climate Change 2013: The Physical Science Basis Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds.)].
Bourtsoukidis E, Bonn B, Noe SM (2014) On-line field measurements of BVOC emissions from Norway spruce (Picea abies) at the hemi-boreal SMEAR-Estonia site under autumn conditions. Boreal environment research 19: 153–
167.
Chameides WL (1989) The chemistry of ozone deposition to plant leaves: role of ascorbic acid. Environmental Science and Technology 23: 595–600.
Chinellato F, Faccoli M, Marini L, Batti A (2014) Distribution of Norway spruce bark and wood boring beetles along Alpine elevational gradients. Agricultural and Forest Entomology 16: 111–118.
Cognato AI (2015) Biology, systematics and evolution of Ips. In:
Vega FE, Hofstetter RW (Eds.) Bark beetles: biology and ecology of native and invasive species. Academic Press Oxford, UK, pp 351–370.
Constable JVH, Litvak ME, Greenberg JP, Monson RK (1999) Monoterpene emission from coniferous trees in response to elevated CO2 concentration and climate warming.
Global Change Biology 5: 252–267.
Copolovici L, Niinemets Ü (2010) Flooding induced emissions of volatile signalling compounds in three tree species with differing waterlogging tolerance. Plant Cell and Environment 33: 1582–1594.
Copolovici L, Kännaste A, Remmel T, Vislap V, Niinemets Ü (2011) Volatile emissions from Alnus glutinosa induced by herbivory are quantitatively related to the extent of damage. Journal of Chemical Ecology 37: 18–28.
Dale VH, Joyce LA, McNulty S, Neilson RP, Ayres MP, Flannigan MD, Hanson PJ, Irland LC, Lugo AE, Peterson CJ, Simberloff D, Swanson FJ, Stocks BJ, Wotton BM (2001) Climate change and forest disturbances. BioScience 51:
723–734
Dalias P, Anderson JM, Bottner P, Couteaux MM (2002) Temperature responses of net nitrogen mineralization and nitrification in conifer forest soils incubated under
standard laboratory conditions. Soil Biology and Biochemistry 34: 691–701.
Dicke M (2009) Behavioural and community ecology of plants that cry for help. Plant Cell and Environment 32: 654–665.
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science 15: 167–175.
Dicke M, Loreto F (2010) Induced plant volatiles: from genes to climate change. Trends in Plant Science 15: 115–117.
Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Critical Reviews in Plant Sciences 25: 417–440.
Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytologist 198: 16–32.
Ehn M, Thornton JA, Kleist E, Sipila M, Junninen H, Pullinen I, Springer M, Rubach F, Tillmann R, Lee B, Lopez Hilfiker F, Andres S, Acir IH, Rissanen M, Jokinen T, Schobesberger S, Kangasluoma J, Kontkanen J, Nieminen T, Kurten T, Nielsen LB, Jorgensen S, Kjaergaard HG, Canagaratna M, Dal Maso M, Berndt T, Petaja T, Wahner A, Kerminen VM, Kulmala M, Worsnop DR, Wildt J, Mentel TF (2014) A large source of low-volatility secondary organic aerosol.
Nature 506: 476–479.
Feussner I, Wasternack C (2002) The lipoxygenase pathway.
Annual Review of Plant Biology 53: 275–297.
Filella I, Wilkinson MJ, Llusià J, Hewitt CN, Peñuelas J (2007) Volatile organic compounds emissions in Norway spruce (Picea abies) in response to temperature changes.
Physiologia Plantarum 130: 58–66.
Ghirardo A, Koch K, Taipale R, Zimmer I, Schnitzler JP, Rinne J (2010) Determination of de novo and pool emissions of terpenes from four common boreal/alpine trees by 13CO2 labelling and PTR-MS analysis. Plant Cell and Environment 33: 781–792.
Gray DR (2008) The relationship between climate and outbreak characteristics of the spruce budworm in eastern Canada.
Climatic Change 87: 361–383.
Gray CM, Monson RK, Fierer N (2010) Emissions of volatile organic compounds during the decomposition of plant litter. Journal of Geophysical Research-Biogeosciences 115:
2156–2202.
Grote R, Monson RK, Niinemets Ü (2013) Leaf-level models of constitutive and stress-driven volatile organic compound emissions. In: Niinemets Ü, Monson RK (Eds.) Biology, controls and models of tree volatile organic compound emissions. Berlin: Springer Science + Business Media BV, 315–355.
Guenther AB, Jiang X, Heald CL, Sakulyanontvittaya T, Duhl T, Emmons LK, Wang X (2012) The Model of Emissions of Gases and Aerosols from Nature version 21 (MEGAN21):
an extended and updated framework for modelling biogenic emissions. Geoscientific Model Development 5:
1471–1492.
Hao G, Romakkaniemi S, Yli-Pirilä P, Joutsensaari J, Kortelainen A, Kroll JH, Miettinen P, Vaattovaara P, Tiitta P, Jaatinen A, Kajos MK, Holopainen JK, Heijari J, Rinne J, Kulmala M, Worsnop DR, Smith JN, Laaksonen A (2011) Mass yields of secondary organic aerosols from the oxidation of -pinene and real plant emissions. Atmospheric Chemistry and Physics 11: 1367–1378.
Hartikainen K, Nerg AM, Kivimäenpää M, Kontunen-Soppela S, Mäenpää M, Oksanen E, Rousi M, Holopainen T (2009) Emissions of volatile organic compounds and leaf structural characteristics of European aspen (Populus tremula) grown under elevated ozone and temperature.
Tree Physiology 29: 1163–1173.
Hartmann DL, Klein Tank AMG, Rusticucci M, Alexander L, Brönnimann S, Charabi Y, Dentener F, Dlugokencky E, Easterling D, Kaplan A, Soden B, Thorne P, Wild M, Zhai PM (2013) Observations: Atmosphere and Surface. In:
Climate Change 2013: The Physical Science Basis
Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (Eds.)].
Cambridge University Press, Cambridge United Kingdom and New York, NY USA.
Hayward S, Tani A, Owen SM, and Hewitt CN (2004) Online analysis of volatile organic compound emissions from Sitka spruce (Picea sitchensis). Tree Physiology 24: 721–728.
Heiden AC, Hoffmann T, Kahl J, Kley D, Klockow D, Langebartels C, Mehlhorn H, Sandermann Jr. H, Schraudner M, Schuh G, Wildt J (1999) Emission of volatile organic compounds from ozone-exposed plants.
Ecological Applications 9: 1160–1167.
Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends in Ecology and Evolution 25: 137–144.
Heijari J, Blande JD, Holopainen JK (2011) Feeding of large pine weevil on Scots pine stem triggers localised bark and systemic shoot emission of volatile organic compounds.
Environmental and Experimental Botany 71: 390 398.
Helmig D, Ortega J, Duhl T, Tanner D, Guenther A, Harley P, Wiedinmyer C, Milford J, Sakulyanontvittaya T (2007) Sesquiterpene emissions from pine trees – identifications, emission rates and flux estimates for the contiguous United States. Environmental Science and Technology 41:
1545–1553.
Holopainen JK, Kainulainen P (2004) Reproductive capacity of the grey pine aphid and allocation response of Scots pine seedlings across temperature gradients: a test of hypotheses predicting outcomes of global warming.
Canadian Journal of Forest Research 34: 94–102.
Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends in Plant Science 15:
176 184.
Holopainen JK, Rikala R, Kainulainen P, Oksanen J (1995) Resource partitioning to growth storage and defence in
nitrogen-fertilized Scots pine and susceptibility of the seedlings to the tarnished plant bug Lygus rugulipennis.
New Phytologist 131: 521–532.
Holopainen JK, Nerg AM, Blande JD (2013) Multitrophic signalling in polluted atmospheres. In: Niinemets Ü, Monson RK (Eds.) Biology, controls and models of tree volatile organic compound emissions. Springer Berlin, pp 285–314.
Högberg MN, Bååth E, Nordgren A, Arnebrant K, Högberg P (2003) Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and saprotrophs – a hypothesis based on field observations in boreal forest.
New Phytologist 160: 225–238.
Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compounds emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)- -caryophyllene, is a defense against a bacterial pathogen. New Phytologist 193: 997–1008.
Huttunen S, Manninen S (2013) A review of ozone responses in Scots pine (Pinus sylvestris). Environmental and Experimental Botany 90: 17–31.
Hyvönen R, Ågren GI, Linder S, Persson T, Cotrufo MF, Ekblad A, Freeman M, Grelle A, Janssens IA, Jarvis PG, Kellomäki S, Lindroth A, Loustau D, Lundmark T, Norby RJ, Oren R, Pilegaard K, Ryan MG, Sigurdsson BD, Strömgren M, van Oijen M, Wallin G (2007) The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytologist 173: 463–480.
IPCC (2014) Climate Change 2014: Synthesis Report Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, Pachauri RK, Meyer LA (Eds.)]. IPCC, Geneva, Switzerland, 151 pp.
Isidorov VA, Smolewska M, Tyszkiewicz Z (2010) Chemical composition of volatile and extractive compounds of pine
and spruce leaf litter in the initial stages of decomposition.
Biogeosciences 7: 2785–2794.
Jakobsen HB, Olsen CE (1994) Influence of climatic factors on emission of flower volatiles in situ. Planta 192: 365–371.
Janson RW (1993) Monoterpene emissions from Scots pine and Norwegian spruce. Journal of Geophysical Research 98:
2839–2850.
Jokinen T, Berndt T, Makkonen R, Kerminen VM, Junninen H, Paasonen P, Stratmann F, Herrmann H, Guenther AB, Worsnop DR, Kulmala M, Ehn M, Sipilä M (2015) Production of extremely low volatile organic compounds from biogenic emissions: Measured yields and atmospheric implications. Proceedings of the National Academy of Sciences-USA 112: 7123–7128.
Joutsensaari J, Yli-Pirilä P, Korhonen H, Arola A, Blande JD, Heijari J, Kivimäenpää M, Mikkonen S, Hao L, Miettinen P, Lyytikäinen-Saarenmaa P, Faiola CL, Laaksonen A, Holopainen JK (2015) Biotic stress accelerates formation of climate-relevant aerosols in boreal forests. Atmospheric Chemistry and Physics 15: 12139–12157.
Jönsson A, Appelberg G, Harding S, Bärring L (2009) Spatio-temporal impact of climate change on the activity and voltinism of the spruce bark beetle Ips typographus. Global Change Biology 15: 486–499.
Kajos MK, Rantala P, Hill M, Hellen H, Aalto J, Patokoski J, Taipale R, Hoerger CC, Reimann S, Ruuskanen TM, Rinne J, Petäjä T (2015) Ambient measurements of aromatic and oxidized VOCs by PTR-MS and GC-MS: intercomparison between four instruments in a boreal forest in Finland.
Atmospheric Measurement Techniques 8: 4453–4473.
Kasischke ES (2000) Boreal ecosystems in the global carbon cycle.
In: Kasischke ES, Stocks BJ (Eds.) Fire, climate change and carbon cycling in the boreal forest. Springer-Verlag, New York, pp 19–30.
Kännaste A, Copolovici L, Pazouki L, Suhhorutšenko M, Niinemets Ü (2013) Highly variable chemical signatures
over short spatial distances among Scots pine (Pinus sylvestris) populations. Tree Physiology 33: 374–387.
Kärvemo S, Schroeder LM (2010) A comparison of outbreak dynamics of the spruce bark beetle in Sweden and the mountain pine beetle (Curculionidae: Scolytinae) in Canada. Entomologisk tidsskrift 131: 215–224.
Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): An overview on emission physiology and ecology. Journal of Atmospheric Chemistry 33: 23 88.
Kesselmeier J, Ciccioli P, Kuhn U, Stefani P, Biesenthal T, Rottenberger S, Wolf A, Vitullo M, Valentini R, Nobre A, Kabat P, Andreae MO (2002) Volatile organic compound emissions in relation to plant carbon fixation and the terrestrial carbon budget. Global Biogeochemical Cycles 16 (4): 1126. DOI: 10.1029/2001GB001813.
Kivimäenpää M, Riikonen J, Ahonen V, Tervahauta A, Holopainen T (2013) Sensitivity of Norway spruce physiology and terpenoid emission dynamics to elevated ozone and elevated temperature under open-field exposure. Environmental and Experimental Botany 90: 32–
42.
Kjellström E (2004) Recent and future signatures of climate change in Europe. Ambio 33: 193–198.
Kleist E, Mentel TF, 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.
Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Botanical Review 72: 1–120.
Kollberg I, Bylund H, Schmidt A, Gershenzon J, Björkman C (2013) Multiple effects of temperature, photoperiod and food quality on the performance of a pine sawfly.
Ecological Entomology 38: 201–208.
Komenda M, Koppmann R (2002) Monoterpene emissions from Scots pine (Pinus sylvestris): Field studies of emission rate
variabilities. Journal Geophysical Research [Atmosphere]
107: ACH 1-1–ACH 1-13.
Komenda M, Kobel K, Koppmann R, Wildt J (2003) Comparability of biogenic VOC emission rate measurements under laboratory and ambient conditions at the example of monoterpene emissions from Scots pine (Pinus sylvestris). Journal of Atmospheric Chemistry 45: 1–
23.
Korhonen JFJ, Pihlatie M, Pumpanen J, Aaltonen H, Hari P, Levula J, Kieloaho AJ, Nikinmaa E, Vesala T, Ilvesniemi H (2013) Nitrogen balance of a boreal Scots pine forest.
Biogeosciences 10: 1083–1095.
Kovalchuk A, Raffaello T, Jaber E, Keriö S, Ghimire RP, Lorenz WW, Dean JF, Holopainen JK, Asiegbu FO (2015) Activation of defence pathways in Scots pine bark after feeding by pine weevil (Hylobius abietis). BMC genomics 16:
352.
Kurkela T, Aalto T, Varama M, Jalkanen R (2005) Defoliation by the common pine sawfly (Diprion pini) and subsequent growth reduction in Scots pine: A retrospective approach.
Silva Fennica 39: 467 480.
Laothawornkitkul J, Taylor JE, Paul ND, Hewitt CN (2009) Biogenic volatile organic compounds in the earth system.
New Phytologist 183: 27 51.
Lerdau M, Matson P, Fall R, Monson R (1995) Ecological controls over monoterpene emissions from Douglas-fir (Pseudotsuga menziesii). Ecology 76: 2640–2647.
Lin C, Owen SM, Peñuelas J (2007) Volatile organic compounds in the roots and rhizosphere of Pinus spp. Soil Biology and Biochemistry 39: 951–960.
Long SP, Naidu SL (2002) Effects of oxidants at the biochemical cell and physiological levels with particular reference to ozone. In: Bell JNB, Treshow M (Eds.) Air pollution and plant life. Wiley, London, pp 69–88.
Loreto F, Schnitzler J (2010) Abiotic stresses and induced BVOCs. Trends in Plant Science 15: 154–166.
Loreto F, Nascetti P, Graverini A, Mannozzi M (2000) Emission and content of monoterpenes in intact and wounded needles of the Mediterranean pine, Pinus pinea. Functional Ecology 14: 589–595.
Loreto F, Fischbach RJ, Schnitzler JP, Ciccioli P, Brancaleoni E, Calfapietra C, Seufert G (2001) Monoterpene emission and monoterpene synthase activities in the Mediterranean evergreen oak Quercus ilex (L.) grown at elevated CO2 concentrations. Global Change Biology 7: 709–717.
Ludley KE, Jickells SM, Chamberlain PM, Whitaker J, Robinson CH (2009) Distribution of monoterpenes between organic resources in upper soil horizons under monocultures of Picea abies, Picea sitchensis and Pinus sylvestris. Soil Biology and Biochemistry 41: 1050–1059.
Lusebrink I, Evenden ML, Blanchet FG, Cooke JEK, Erbilgin N (2011) Effect of water stress and fungal inoculation on monoterpene emission from a historical and a new pine host of the mountain pine beetle. Journal of Chemical Ecology 37: 1013–1026.
Lyytikäinen-Saarenmaa P (1999) Growth responses of Scots pine (Pinaceae) to artificial and sawfly (Hymenoptera:
Diprionidae) defoliation. Canadian Entomologist 131:
455 463.
Lyytikäinen-Saarenmaa P, Tomppo E (2002) Impact of sawfly defoliation on growth of Scots pine Pinus sylvestris (Pinaceae) and associated economic losses. Bulletin of Entomological Research 92: 137 140.
Machacova K, Papen H, Kreuzwieser J, Rennenberg H (2013) Inundation strongly stimulates nitrous oxide emissions from stems of the upland tree Fagus sylvatica and the riparian tree Alnus glutinosa. Plant Soil 364: 287–301.
Machacova K, Bäck J, Vanhatalo A, Halmeenmäki E, Kolari P, Mammarella I, Pumpanen J, Acosta M, Urban O, Pihlatie M (2016) Pinus sylvestris as a missing source of nitrous oxide and methane in boreal forest. Scientific Reports 6:
23410.
Maja MM, Kasurinen A, Yli-Pirilä P, Joutsensaari J, Klemola T, Holopainen T, Holopainen JK (2014) Contrasting responses of silver birch VOC emissions to short-and long-term herbivory. Tree Physiology 34: 241–252.
Makoto K, Koike T (2007) Effects of nitrogen supply on photosynthetic and anatomical changes in current-year needles of Pinus koraiensis seedlings grown under two irradiances. Phytosynthetica 45: 99–104.
Martin D, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiology 129:
1003–1018.
Matsui K, Sugimoto K, Mano J, Ozawa R, Takabayashi J (2012) Differential metabolisms of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements. PLoS ONE 7(4): e36433.
Matyssek R, Sandermann H (2003) Impact of ozone on trees: an ecophysiological perspective. In: Esser K, Lüttge U, Beyschlag W, Hellwig F (Eds.) Progress in Botany 64: 349–
404. Springer-Verlag Berlin Heidelberg, pp XV 536.
McGarvey DJ, Croteau R (1995) Terpenoid metabolism. Plant Cell 7: 1015–1026.
Niemelä P, Chapin FS, Danell K, and Bryant JP (2001) Herbivory-mediated responses of selected boreal forests to climatic change. Climate Change 48: 427–440.
Niinemets Ü (2010) Mild versus severe stress and BVOCs:
thresholds, priming and consequences. Trends in Plant Science 15: 145–153.
Niinemets Ü, Kännaste A, Copolovici L (2013) Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage. Frontiers in Plant Science 4: 262.
Oliet JA, Puértolas J, Planelles R, Jacobs DF (2013) Nutrient loading of forest tree seedlings to promote stress resistance and field performance: a Mediterranean perspective. New Forests 44: 649–669.
Ollinger SV, Aber JD, Reich PB, Freuder RJ (2002) Interactive effects of nitrogen deposition, tropospheric ozone, elevated CO2 and land use history on the carbon dynamics of northern hardwood forests. Global Change Biology 8:
545–562.
Ortega J, Helmig D (2008) Approaches for quantifying reactive and low-volatility biogenic organic compound emissions by vegetation enclosure techniques-Part A. Chemosphere 72: 343–364.
Öhrn P, Långström B, Lindelöw Å, Björklund N (2014) Seasonal flight patterns of Ips typographus in southern Sweden and thermal sums required for emergence. Agricultural and Forest Entomology 16: 147–157.
Paré PW, Tumlinson JH (1997) Induced synthesis of plant volatiles. Nature 385: 30–31.
Pegoraro E, Rey A, Barron-Gafford G, Monson RK, Malhi Y, Murthy R (2004) Effect of elevated CO2 concentration and vapour pressure deficit on isoprene emission from leaves of Populus deltoides during drought. Functional Plant Biology 31: 1137–1147.
Peñuelas J, Llusià J (2003) BVOCs: plant defense against climate warming? Trends in Plant Science 8: 105–109.
Peñuelas J, Staudt M (2010) BVOCs and global change. Trends in Plant Science 15: 133–144.
Pichersky E, Noel J, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311(5762): 808–811.
Pihlatie M, Pumpanen J, Rinne J, Ilvesniemi H, Simojoki A, Hari P, Vesala T (2007) Gas concentration driven fluxes of nitrous oxide and carbon dioxide in boreal forest soil.
Tellus B 59: 458–469.
Pinto DM, Blande JD, Nykänen R, Dong WX, Nerg AM, Holopainen JK (2007) Ozone degrades common herbivore-induced plant volatiles: Does this affect herbivore prey location by predators and parasitoids? Journal of Chemical
Pinto DM, Blande JD, Nykänen R, Dong WX, Nerg AM, Holopainen JK (2007) Ozone degrades common herbivore-induced plant volatiles: Does this affect herbivore prey location by predators and parasitoids? Journal of Chemical