Abstract
Elevated O3 levels can strongly impair the health and vitality of forest ecosystems. Free-air exposure systems reveal that forest tree and stand growth can be reduced strongly under chronic O3 stress. Detailed knowledge of the effect of O3 exposure on photosynthesis, carbon sequestration, allometry and growth during chronic stress is available. However, knowledge of growth response after O3 reduction is scarce. Here, we analyse the growth of mature Norway spruce (Picea abies (L.) Karst.) and European beech (Fagus sylvatica L.) in the free-air O3 fumigation experiment at Kranzberg Forest. We compare tree growth over a 9-year period (2008–2016) after exposure to O3 (2000–2007). During 2 × O3 exposure, the annual basal area growth of Norway spruce and European beech decreased by 24 and 32%, respectively. After cessation of 2 × O3 exposure, the annual basal area growth of Norway spruce and European beech not only recovered but exceeded the growth of the trees in the control condition by 14 and 24%, respectively. The growth resilience and resistance of trees previously exposed to 2 × O3 towards drought stress and late frost was hardly lower than that of the trees in the control condition. The capacity for growth recovery even after long-term chronic O3 stress emphasizes the strong beneficial effect of air pollution control on the health of forest ecosystems and on the global land carbon sink.
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References
Alonso R, Elvira S, Castillo FJ, Gimeno BS (2001) Interactive effects of ozone and drought stress on pigments and activities of antioxidative enzymes in Pinus halepensis. Plant Cell Environ 24(9):905–916
Assmann E (1961) Waldertragskunde. Organische Produktion, Struktur, Zuwachs und Ertrag von Waldbeständen. BLV Verlagsgesellschaft, München, Bonn, Wien, 490 p
Association of German Forest Research Organizations (1988) [Deutscher Verband Forstlicher Forschungsanstalten] Empfehlungen zur ertragskundlichen Aufnahme- und Auswertungsmethodik für den Themenkomplex „Waldschäden und Zuwachs“. Allgemeine Forst- und Jagdzeitung 159:115–116
Barbo DN, Chappelka AH, Somers GL, Miller-Goodman MS, Stolte K (1998) Diversity of an early successional plant community as influenced by ozone. New Phytol 138(4):653–662
Bassin S, Volk M, Suter M, Buchmann N, Fuhrer J (2007) Nitrogen deposition but not ozone affects productivity and community composition of subalpine grassland after 3 yr of treatment. New Phytol 175(3):523–534
Botkin DB, Smith WH, Carlson RW, Smith TL (1972) Effects of ozone on white pine saplings: variation in inhibition and recovery of net photosynthesis. Environ Pollut (1970) 3(4):273–289
Braun S, Schindler Ch, Rihm B, Flückiger W (2007) Shoots growth of mature Fagus sylvatica and Picea abies in relation to ozone. Environ Pollut 146:624–628
Chappelka AH, Samuelson LJ (1998) Ambient ozone effects on forest trees of the eastern United States: a review. New Phytol 139(1):91–108
Constable JV, Taylor GE Jr, Laurence JA, Weber JA (1996) Climatic change effects on the physiology and growth of Pinus ponderosa: expectations from simulation modeling. Can J For Res 26(8):1315–1325
Cooley DR, Manning WJ (1987) The impact of ozone on assimilate partitioning in plants: a review. Environ Pollut 47(2):95–113
Crawley MJ (2009) The R book, Reprint. with corr. Wiley, Chichester
De Marco A, Screpanti A, Attorre F, Proietti C, Vitale M (2013) Assessing ozone and nitrogen impact on net primary productivity with a generalised non-linear model. Environ Pollut 172:250–263
de Martonne E (1926) Une novelle fonction climatologique: L’indice d’aridité. La Météorologie 21:449–458
Dickson RE, Coleman MD, Pechter P, Karnosky D (2001) Growth and crown architecture of two aspen genotypes exposed to interacting ozone and carbon dioxide. Environ Pollut 115(3):319–334
Dobbertin M (2005) Tree growth as indicator of tree vitality and of tree reaction to environmental stress: a review. Eur J For Res 124(4):319–333
Felzer BS, Kicklighter D, Melillo J, Wang C, Zhuang Q, Prinn R (2004) Effects of ozone on net primary production and carbon sequestration in the conterminous United States using a biogeochemistry model. Tellus B 56(3):230–248
Felzer BS, Cronin T, Reilly JM, Melillo JM, Wang X (2007) Impacts of ozone on trees and crops. Comptes Rendus Geosci 339(11):784–798
Gao F, Catalayud V, Paoletti E, Hoshika Y, Feng Z (2017) Water stress mitigates the negative effects of ozone on photosynthesis and biomass in poplar plants. Environ Pollut 230(Supplement C):268–279
Grantz DA, Gunn S, Vu HB (2006) O3 impacts on plant development: a meta-analysis of root/shoot allocation and growth. Plant, Cell Environ 29(7):1193–1209
Grünhage L, Matyssek R, Häberle K-H, Wieser G, Metzger U, Leuchner M, Raspe S (2012) Flux-based ozone risk assessment for adult beech forests. Trees 26(6):1713–1721
Günthardt-Goerg MS, Vollenweider P (2007) Linking stress with macroscopic and microscopic leaf response in trees: new diagnostic perspectives. Environ Pollut 147(3):467–488
Häberle K-H, Weigt R, Nikolova PS, Reiter IM, Cermak J, Wieser G, Blaschke H, Rötzer T, Pretzsch H, Matyssek R (2012) Case Study “Kranzberger Forst”: Growth and Defence in European Beech (Fagus sylvatica L.) and Norway Spruce (Picea abies (L.) Karst). In: Matyssek R et al (eds) Growth and defence in plants, ecological studies, vol 220. Springer, Berlin, pp 243–271. https://doi.org/10.1007/978-3-642-30645-7_11
Hom JL, Oechel WC (1983) The photosynthetic capacity, nutrient content, and nutrient use efficiency of different needle age-classes of black spruce (Picea mariana) found in interior Alaska. Can J For Res 13(5):834–839
Isebrands JG, McDonald EP, Kruger E, Hendrey G, Percy K, Pregitzer K, Karnosky DF (2001) Growth responses of Populus tremuloides clones to interacting elevated carbon dioxide and tropospheric ozone. Environ Pollut 115(3):359–371
Karlsson PE, Medin EL, Wallin G, Selldén G, Skärby L (1997) Effects of ozone and drought stress on the physiology and growth of two clones of Norway spruce (Picea abies). The New Phytol 136(2):265–275
Karlsson PE, Örlander G, Langvall O, Uddling J, Hjorth U, Wiklander K, Areskoug B, Grennfelt P (2006) Negative impact of ozone on the stem basal area increment of mature Norway spruce in south Sweden. For Ecol Manag 232:146–151
Karnosky DF, Werner H, Holopainen T, Percy K, Oksanen T, Oksanen E, Cox R (2007) Free-air exposure systems to scale up ozone research to mature trees. Plant Biol 9(02):181–190
Kress LW, Skelly JM, Hinkelmann KH (1982) Growth impact of O3, NO2 and/or SO2 on Pinus taeda. Environ Monit Assess 1(3):229–239
Lloret F, Keeling EG, Sala A (2011) Components of tree resilience: effects of successive low-growth episodes in old ponderosa pine forests. Oikos 120:1909–1920
Löw M, Herbinger K, Nunn AJ, Häberle K-H, Leuchner M, Heerdt C, Matyssek R (2006) Extraordinary drought of 2003 overrules ozone impact on adult beech trees (Fagus sylvatica). Trees 20(5):539–548
LWF (2017) Bayerische Waldklimastationen (WKS) Bayerische Landesanstalt für Wald und Forstwirtschaft, http://www.lwf.bayern.de/wks, 09. July 2017
Manning WJ (2005) Establishing a cause and effect relationship for ambient ozone exposure and tree growth in the forest: progress and an experimental approach. Environ Pollut 137(3):443–454
Martínez-Vilalta J, López BC, Loepfe L, Lloret F (2012) Stand-and tree-level determinants of the drought response of Scots pine radial growth. Oecologia 168(3):877–888
Matyssek R, Sandermann H (2003) Impact of ozone on trees: an ecophysiological perspective. Progress in botany, 349-404
Matyssek R, Schnyder H, Elstner EF, Munch JC, Pretzsch H, Sandermann H (2002) Growth and parasite defence in plants; the balance between resource sequestration and retention: in lieu of a guest editorial. Plant Biol 4(02):133–136
Matyssek R, Wieser G, Ceulemans R, Rennenberg H, Pretzsch H, Haberer K, Löw M, Nunn AJ, Werner H, Wipfler P, Oßwald W, Nikolova P, Hanke DE, Kraigher H, Tausz M, Bahnweg G, Kitao M, Dieler J, Sandermann H, Herbingerm K, Grebenc T, Blumenröther M, Deckmyn G, Grams TEE, Heerdt C, Leuchner M, Fabian P, Häberle K-H (2010) Enhanced ozone strongly reduces carbon sink strength of adult beech (Fagus sylvatica) Resume from the free-air fumigation study at Kranzberg Forest. Environ Pollut 158(8):2527–2532
Matyssek R, Clarke N, Cudlín P, Mikkelsen TN, Tuovinen JP, Wieser G, Paoletti E (2013) Climate change, air pollution and global challenges: understanding and perspectives from forest research, vol 13. Elsevier, Newnes
Matyssek R, Kozovits AR, Schnitzler JP, Pretzsch H, Dieler J, Wieser G (2014) Forest trees under air pollution as a factor of climate change. In: Tausz M, Grulke N (eds) Trees in a changing environment. Springer, Dordrecht, pp 117–163
McLaughlin SB, McConathy RK, Duvick D, Mann LK (1982) Effects of chronic air pollution stress on photosynthesis, carbon allocation, and growth of white pine trees. For Sci 28(1):60–70
McLaughlin SB, Nosal M, Wullschleger SD, Sun G (2007) Interactive effects of ozone and climate on tree growth and water use in a southern Appalachian forest in the USA. New Phytol 174(1):109–124
Merlin M, Perot T, Perret S, Korboulewsky N, Vallet P (2015) Effects of stand composition and tree size on resistance and resilience to drought in sessile oak and Scots pine. For Ecol Manag 339:22–33
Niinemets Ü (2010) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. For Ecol Manage 260(10):1623–1639
Nunn AJ, Weiser G, Reiter IM, Häberle KH, Grote R, Havranek WM, Matyssek R (2006) Testing the unifying theory of ozone sensitivity with mature trees of Fagus sylvatica and Picea abies. Tree Physiol 26(11):1391–1403
Pääkkönen E, Paasisalo S, Holopainen T, Kärenlamp L (1993) Growth and stomatal responses of birch (Betula pendula Roth.) clones to ozone in open-air and chamber fumigations. New Phytol 125(3):615–623
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) nlme: Linear and Nonlinear Mixed Effects Model
Pretzsch H, Dieler J (2011) The dependency of the size-growth relationship of Norway spruce (Picea abies [L.] Karst.) and European beech (Fagus sylvatica [L.]) in forest stands on long-term site conditions, drought events, and ozone stress. Trees 25(3):355–369
Pretzsch H, Utschig H (1989) Das “Zuwachstrend-Verfahren” für die Abschätzung krankheitsbedingter Zuwachsverluste auf den Fichten- und Kiefern-Weiserflächen in den bayerischen Schadgebieten. Forstarchiv 60:188–193
Pretzsch H, Kahn M, Grote R (1998) Die Fichten-Buchen-Mischbestände des Sonderforschungsbereiches »Wachstum oder Parasitenabwehr?« im Kranzberger Forst. Forstwissenschaftliches Centralblatt 117:241–257
Pretzsch H, Dieler J, Matyssek R, Wipfler P (2010) Tree and stand growth of mature Norway spruce and European beech under long-term ozone fumigation. Environ Pollut 158(4):1061–1070
Pretzsch H, Schütze G, Uhl E (2012) Resistance of European tree species to drought stress in mixed versus pure forests: evidence of stress release by inter-specific facilitation. Plant Biol 15:483–495
Pretzsch H, Schütze G, Uhl E (2013) Resistance of European tree species to drought stress in mixed versus pure forests: evidence of stress release by inter-specific facilitation. Plant Biol 15:483–495
Pretzsch H, Rötzer T, Matyssek R, Grams TEE, Häberle K-H, Pritsch K, Kerner R, Munch JC (2014) Mixed Norway spruce (Picea abies [L.] Karst) and European beech (Fagus sylvatica [L.]) stands under drought: from reaction pattern to mechanism. Trees Struct Funct 28:1305–1321
Quan C, Han S, Utescher T, Zhang C, Liu YS (2013) Validation of temperature–precipitation based aridity index: paleoclimatic implications. Palaeogeogr Palaeoclimatol Palaeoecol 386:86–95
Retzlaff WA, Weinstein DA, Laurence JA, Gollands B (1997) Simulating the growth of a 160-year-old sugar maple (Acer saccharum) tree with and without ozone exposure using the TREGRO model. Can J For Res 27(5):783–789
Retzlaff WA, Arthur MA, Grulke NE, Weinstein DA, Gollands B (2000) Use of a single-tree simulation model to predict effects of ozone and drought on growth of a white fir tree. Tree Physiol 20(3):195–202
Rötzer T, Seifert T, Gayler S, Priesack E, Pretzsch H (2012) Effects of stress and defence allocation on tree growth: simulation results at the individual and stand level. In: Matyssek R et al (eds) Growth and defence in plants: resource allocation at multiple scales. Ecological studies, vol 220. Springer, Berlin, pp 401–432
Rötzer T, Häberle K-H, Kallenbach C, Matyssek R, Schütze G, Pretzsch H (2017) Tree species and size drive water consumption of beech/spruce forests—a simulation study highlighting growth under water limitation. Plant Soil. https://doi.org/10.1007/s11104-017-3306-x
Sitch S, Cox PM, Collins WJ, Huntingford C (2007) Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature 448(7155):791–794
Somers GL, Chappelka AH, Rosseau P, Renfo JR (1998) Empirical evidence of growth decline related to visible ozone injury. For Ecol Manag 104:129–137
Thurm EA, Uhl E, Pretzsch H (2016) Mixture reduces climate sensitivity of Douglas-fir stem growth. For Ecol Manag 376:205–220
Vollenweider P, Woodcock H, Keltry MJ, Hofer R-M (2003) Reduction of stem growth and site dependency of leaf injury in Massachusetts black cherries exhibiting ozone symptoms. Environ Pollut 125:467–480
Wang K, Kellomäki S, Laitinen K (1995) Effects of needle age, long-term temperature and CO2 treatments on the photosynthesis of Scots pine. Tree Physiol 15(4):211–218
Weber JA, Clark CS, Hogsett WE (1993) Analysis of the relationships among O3 uptake, conductance, and photosynthesis in needles of Pinus ponderosa. Tree Physiol 13(2):157–172
Weinstein DA, Samuelson LJ, Arthur MA (1998) Comparison of the response of red oak (Quercus rubra) seedlings and mature trees to ozone exposure using simulation modeling. Environ Pollut 102(2):307–320
Werner H, Fabian P (2002) Free-air fumigation of mature trees. Environ Sci Pollut Res 9:117–121
Wipfler P, Seifert T, Heerdt C, Werner H, Pretzsch H (2005) Growth of adult Norway spruce (Picea abies [L.] Karst.) and European beech (Fagus sylvatica L.) under free-air ozone fumigation. Plant Biol 7(6):611–618
Wittig VE, Ainsworth EA, Naidu SL, Karnosky DF, Long SP (2009) Quantifying the impact of current and future tropospheric ozone on tree biomass, growth, physiology and biochemistry: a quantitative meta-analysis. Global Change Biol 15(2):396–424
Zimmermann L, Raspe S, Grimmeisen W (2012) 2011—die Fortsetzung der warmen Jahre. LWF aktuell 87:40–43
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer, New York
Acknowledgements
Thanks to the Bavarian State Ministry for Nutrition, Agriculture, and Forestry for permanent support of the project W 07 “Long-term experimental plots for forest growth and yield research” (# 7831-22209-2013), to Bayerische Staatsforsten (BaySF) for supporting the establishment of the plots, and to the German Science Foundation and the Bavarian State Ministry of the Environment and Consumer Protection for providing the funds for the projects PR 292/12-1 “Tree and stand-level growth reactions on drought in mixed versus pure forests of Norway spruce and European beech”. Thanks are also due to Manuela Baumgarten for providing the time series of the ambient O3 concentration for Fig. 1, to Laura Zeller for assisting in the data evaluation, to Ulrich Kern for the graphical artwork, to Charlotte Pretzsch for English language revision and to the anonymous reviewers for improving the manuscript through constructive criticism.
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HP initiated the study and wrote the manuscript. GS carried out the field work and the data analyses.
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Communicated by Rüdiger Grote.
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Pretzsch, H., Schütze, G. Growth recovery of mature Norway spruce and European beech from chronic O3 stress. Eur J Forest Res 137, 251–263 (2018). https://doi.org/10.1007/s10342-018-1106-3
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DOI: https://doi.org/10.1007/s10342-018-1106-3