Atmospheric pollution critically affects forest ecosystems around the world by directly impacting the assimilation apparatus of trees and indirectly by altering soil conditions, which subsequently also leads to changes in carbon cycling. To evaluate the extent of the physiological effect of moderate level sulfate and reactive nitrogen acidic deposition, we performed a retrospective dendrochronological analysis of several physiological parameters derived from periodic measurements of carbon stable isotope composition ((13)C discrimination, intercellular CO2 concentration and intrinsic water use efficiency) and annual diameter increments (tree biomass increment, its inter-annual variability and correlation with temperature, cloud cover, precipitation and Palmer drought severity index). The analysis was performed in two mountain Norway spruce (Picea abies) stands of the Bohemian Forest (Czech Republic, central Europe), where moderate levels of pollution peaked in the 1970s and 1980s and no evident impact on tree growth or link to mortality has been reported. The significant influence of pollution on trees was expressed most sensitively by a 1.88‰ reduction of carbon isotope discrimination (Δ(13)C). The effects of atmospheric pollution interacted with increasing atmospheric CO2 concentration and temperature. As a result, we observed no change in intercellular CO2 concentrations (Ci), an abrupt increase in water use efficiency (iWUE) and no change in biomass increment, which could also partly result from changes in carbon partitioning (e.g., from below- to above-ground). The biomass increment was significantly related to Δ(13)C on an individual tree level, but the relationship was lost during the pollution period. We suggest that this was caused by a shift from the dominant influence of the photosynthetic rate to stomatal conductance on Δ(13)C during the pollution period. Using biomass increment-climate correlation analyses, we did not identify any clear pollution-related change in water stress or photosynthetic limitation (since biomass increment did not become more sensitive to drought/precipitation or temperature/cloud cover, respectively). Therefore, we conclude that the direct effect of moderate pollution on stomatal conductance was likely the main driver of the observed physiological changes. This mechanism probably caused weakening of the spruce trees and increased sensitivity to other stressors.

Department of Forest Ecology Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czech Republic

Faculty of Science University of South Bohemia in České Budějovice České Budějovice Czech Republic

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Bates D., Mächler M., Bolker B., Walker S. (2015). Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67:51 10.18637/jss.v067.i01 DOI

Boettger T., Haupt M., Friedrich M., Waterhouse J. S. (2014). Reduced climate sensitivity of carbon, oxygen and hydrogen stable isotope ratios in tree-ring cellulose of silver fir (Abies alba Mill.) influenced by background SO2 in Franconia (Germany, Central Europe). Environ. Pollut. 185 281–294. 10.1016/j.envpol.2013.10.030 PubMed DOI

Bunn A. G. (2008). A dendrochronology program library in R (dplR). Dendrochronologia 26 115–124. 10.1016/j.dendro.2008.01.002 DOI

Čada V., Morrissey R. C., Michalová Z., Bače R., Janda P., Svoboda M. (2016). Frequent severe natural disturbances and non-equilibrium landscape dynamics shaped the mountain spruce forest in central Europe. For. Ecol. Manage. 363 169–178. 10.1016/j.foreco.2015.12.023 DOI

Cháb J., Stráník Z., Eliáš M. (2007). Geological Map of the Czech Republic 1:500 000. Prague: Czech Geological Survey.

Cook E. R., Peters K. (1997). Calculating unbiased tree-ring indices for the study of climatic and environmental change. Holocene 7 361–370. 10.1177/095968369700700314 DOI

Elling W., Dittmar C., Pfaffelmoser K., Rötzer T. (2009). Dendroecological assessment of the complex causes of decline and recovery of the growth of silver fir (Abies alba Mill.) in Southern Germany. For. Ecol. Manage. 257 1175–1187. 10.1016/j.foreco.2008.10.014 DOI

Emerson J. D. (1983). “Mathematical aspects of transformation,” in Understanding Robust and Exploratory Data Analysis eds Hoaglin D. C., Mosteller F., Tukey J. W. (New York, NY: John Wiley & Sons; ).

Farquhar G., O’Leary M., Berry J. (1982). On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust. J. Plant Physiol. 9 121 10.1071/PP9820121 DOI

Fritts H. C. (1976). Tree Rings and Climate. New York, NY: Academic Press.

Gebauer G., Schulze E. (1991). Carbon and nitrogen isotope ratios in different compartments of a healthy and a declining Picea abies forest in the Fichtelgebirge, NE Bavaria. Oecologia 87 198–207. 10.1007/BF00325257 PubMed DOI

Greaver T. L., Sullivan T. J., Herrick J. D., Barber M. C., Baron J. S., Cosby B. J., et al. (2012). Ecological effects of nitrogen and sulfur air pollution in the US: what do we know? Front. Ecol. Environ. 10:365 10.1890/110049 DOI

Harlow B. A., Marshall J. D., Robinson A. P. (2006). A multi-species comparison of δ13C from whole wood, extractive-free wood and holocellulose. Tree Physiol. 26 767–774. 10.1093/treephys/26.6.767 PubMed DOI

Harris I., Jones P. D., Osborn T. J., Lister D. H. (2014). Updated high-resolution grids of monthly climatic observations - the CRU TS3.10 Dataset. Int. J. Climatol. 34 623–642. 10.1002/joc.3711 DOI

Hauck M., Zimmermann J., Jacob M., Dulamsuren C., Bade C., Ahrends B., et al. (2012). Rapid recovery of stem increment in Norway spruce at reduced SO2 levels in the Harz Mountains, Germany. Environ. Pollut. 164 132–141. 10.1016/j.envpol.2012.01.026 PubMed DOI

Hruška J., Oulehle F., Šamonil P., Šebesta J., Tahovská K., Hleb R., et al. (2012). Long-term forest soil acidification, nutrient leaching and vegetation development: linking modelling and surveys of a primeval spruce forest in the Ukrainian Transcarpathian Mts. Ecol. Modell. 244 28–37. 10.1016/j.ecolmodel.2012.06.025 DOI

Hůnová I., Maznová J., Kurfürst P. (2014). Trends in atmospheric deposition fluxes of sulphur and nitrogen in Czech forests. Environ. Pollut. 184 668–675. 10.1016/j.envpol.2013.05.013 PubMed DOI

Högberg P., Fan H., Quist M., Binkley D., Tamm C. O. (2006). Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Glob. Chang. Biol 12 489–499. 10.1111/j.1365-2486.2006.01102.x DOI

Janda P., Svoboda M., Bače R., Čada V., Peck J. E. (2014). Three hundred years of spatio-temporal development in a primary mountain Norway spruce stand in the Bohemian Forest, central Europe. For. Ecol. Manage. 330 304–311. 10.1016/j.foreco.2014.06.041 DOI

Jentschke G., Drexhage M., Fritz H. W., Fritz E., Schella B., Lee D. H., et al. (2001). Does soil acidity reduce subsoil rooting in Norway spruce (Picea abies)? Plant Soil 237 91–108. 10.1023/A:1013305712465 DOI

Kaňa J., Tahovská K., Kopáček J., Šantrůčková H. (2015). Excess of organic carbon in mountain spruce forest soils after bark beetle outbreak altered microbial N transformations and mitigated N-saturation. PLoS ONE 10:e0134165 10.1371/journal.pone.0134165 PubMed DOI PMC

Kandler O., Innes J. L. (1995). Air pollution and forest decline in Central Europe. Environ. Pollut. 90 171–180. 10.1016/0269-7491(95)00006-D PubMed DOI

Klimont Z., Smith S. J., Cofala J. (2013). The last decade of global anthropogenic sulfur dioxide: 2000–2011 emissions. Environ. Res. Lett. 8:014003 10.1088/1748-9326/8/1/014003 DOI

Knibbe B. (2007). Past4: Personal Analysis System for Treering Research Version 4.2. Vienna: SCIEM.

Kopáček J., Hruška J. (2010). Reconstruction of acidic deposition in the catchments of Plešné and Čertovo lakes (the Bohemian Forest). Silva Gabreta 16 149–163.

Kopáček J., Vrba J. (2006). Integrated ecological research of catchment-lake ecosystems in the Bohemian Forest (Central Europe): a preface. Biologia (Bratisl.) 61 S363–S370.

Lefcheck J. S. (2015). PiecewiseSEM: pecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Ecol. Evol. 10.1111/2041-210X.12512 DOI

Lenth R. (2015). lsmeans: Least-Squares Means. R Package Version 2.21-1. Available at: http://cran.r-project.org/package=lsmeans.

Levanič T., Gričar J., Gagen M., Jalkanen R., Loader N. J., McCarroll D., et al. (2009). The climate sensitivity of Norway spruce [Picea abies (L.) Karst.] in the southeastern European Alps. Trees 23 169–180. 10.1007/s00468-008-0265-0 DOI

McCarroll D., Loader N. (2004). Stable isotopes in tree rings. Quat. Sci. Rev. 23 771–801. 10.1016/j.quascirev.2003.06.017 DOI

McNulty S. G., Swank W. T. (1995). Wood δ13C as a measure of annual basal area growth and soil water stress in a Pinus strobus forest. Ecology 76 1581–1586. 10.2307/1938159 DOI

Meng F. R., Cox R. M., Arp P. A. (1994). Fumigating mature spruce branches with SO2 effects on net photosynthesis and stomatal conductance. Can. J. For. Res. Can. Rech. For. 24 1464–1471. 10.1139/x94-189 DOI

Nakagawa S., Schielzeth H. (2013). A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4 133–142. 10.1111/j.2041-210x.2012.00261.x DOI

Niemelä P., Lumme I., Mattson W., Arkhipov V. (1997). 13C in tree rings along an air pollution gradient in the Karelian Isthmus, northwest Russia and southeast Finland. Can. J. For. Res. 27 609–612. 10.1139/x97-005 DOI

Nilsson L. O., Wallander H. (2003). Production of external mycelium by ectomycorrhizal fungi in a norway spruce forest was reduced in response to nitrogen fertilization. New Phytol. 158 409–416. 10.1046/j.1469-8137.2003.00728.x DOI

Oulehle F., Evans C. D., Hofmeister J., Krejci R., Tahovska K., Persson T., et al. (2011). Major changes in forest carbon and nitrogen cycling caused by declining sulphur deposition. Glob. Chang. Biol. 17 3115–3129. 10.1111/j.1365-2486.2011.02468.x DOI

Peñuelas J., Canadell J. G., Ogaya R. (2011). Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Glob. Ecol. Biogeogr. 20 597–608. 10.1111/j.1466-8238.2010.00608.x DOI

Pregitzer K. S., Euskirchen E. S. (2004). Carbon cycling and storage in world forests: Biome patterns related to forest age. Glob. Chang. Biol. 10 2052–2077. 10.1111/j.1365-2486.2004.00866.x DOI

Primicia I., Camarero J. J., Janda P., Čada V., Morrissey R. C., Trotsiuk V., et al. (2015). Age, competition, disturbance and elevation effects on tree and stand growth response of primary Picea abies forest to climate. For. Ecol. Manage. 354 77–86. 10.1016/j.foreco.2015.06.034 DOI

R Development Core Team (2014). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. 10.1007/978-3-540-74686-74687 DOI

Rinne K. T., Loader N. J., Switsur V. R., Treydte K. S., Waterhouse J. S. (2010). Investigating the influence of sulphur dioxide (SO2) on the stable isotope ratios (δ13C and δ18O) of tree rings. Geochim. Cosmochim. Acta 74 2327–2339. 10.1016/j.gca.2010.01.021 DOI

Rydval M., Wilson R. (2012). The Impact of Industrial SO2 Pollution on North Bohemia Conifers. Water Air Soil Pollut. 223 5727–5744. 10.1007/s11270-012-1310-6 DOI

Sander C., Eckstein D., Kyncl J., Dobrý J. (1995). The growth of spruce (Picea abies (L) Karst) in the Krkonoše-(Giant) Mountains as indicated by ring width and wood density. Ann. Des Sci. For. 52 401–410. 10.1051/forest:19950501 DOI

Šantrůčková H., Šantrůček J., Šetlík J., Svoboda M., Kopáček J. (2007). Carbon isotopes in tree rings of Norway spruce exposed to atmospheric pollution. Environ. Sci. Technol. 41 5778–5782. 10.1021/es07001 PubMed DOI

Saurer M., Spahni R., Frank D. C., Joos F., Leuenberger M., Loader N. J., et al. (2014). Spatial variability and temporal trends in water-use efficiency of European forests. Glob. Chang. Biol. 20 3700–3712. 10.1111/gcb.12717 PubMed DOI

Savard M. M. (2010). Tree-ring stable isotopes and historical perspectives on pollution - an overview. Environ. Pollut. 158 2007–2013. 10.1016/j.envpol.2009.11.031 PubMed DOI

Scheffer M., Bascompte J., Brock W. A., Brovkin V., Carpenter S. R., Dakos V., et al. (2009). Early-warning signals for critical transitions. Nature 461 53–59. 10.1038/nature08227 PubMed DOI

Seedre M., Kopáček J., Janda P., Bače R., Svoboda M. (2015). Carbon pools in a montane old-growth Norway spruce ecosystem in Bohemian Forest: effects of stand age and elevation. For. Ecol. Manage. 346 106–113. 10.1016/j.foreco.2015.02.034 DOI

Svoboda M., Janda P., Nagel T. A., Fraver S., Rejzek J., Bače R. (2012). Disturbance history of an old-growth sub-alpine Picea abies stand in the Bohemian Forest, Czech Republic. J. Veg. Sci. 23 86–97. 10.1111/j.1654-1103.2011.01329.x DOI

Svoboda M., Matějka K., Kopáček J. (2006). Biomass and element pools of understory vegetation in the catchments of Čertovo Lake and Plešné Lake in the Bohemian Forest. Biologia (Bratisl) 61 S509–S521. 10.2478/s11756-007-0074-8 DOI

Svoboda M., Pouska V. (2008). Structure of a Central-European mountain spruce old-growth forest with respect to historical development. For. Ecol. Manage. 255 2177–2188. 10.1016/j.foreco.2007.12.031 DOI

Thomas R. B., Spal S. E., Smith K. R., Nippert J. B. (2013). Evidence of recovery of Juniperus virginiana trees from sulfur pollution after the Clean Air Act. Proc. Natl. Acad. Sci. U.S.A. 110 15319–15324. 10.1073/pnas.1308115110 PubMed DOI PMC

Treml V., Ponocná T., Büntgen U. (2012). Growth trends and temperature responses of treeline Norway spruce in the Czech-Polish Sudetes Mountains. Clim. Res. 55 91–103. 10.3354/cr01122 DOI

Turek J., Fluksová H., Hejzlar J., Kopáček J., Porcal P. (2014). Modelling air temperature in catchments of Čertovo and Plešné lakes in the Bohemian Forest back to 1781. Silva Gabreta 20 1–24.

Viet H. D., Kwak J. H., Lee K. S., Lim S. S., Matsushima M., Chang S. X., et al. (2013). Foliar chemistry and tree ring δ13C of Pinus densiflora in relation to tree growth along a soil pH gradient. Plant Soil 363 101–112. 10.1007/s11104-012-1301-9 DOI

Vrba J., Kopáček J., Fott J., Nedbalova L. (2014). Forest die-back modified plankton recovery from acidic stress. Ambio 43 207–217. 10.1007/s13280-013-0415-5 PubMed DOI PMC

Wilson R. J. S., Luckman B. H., Esper J. (2005). A 500 year dendroclimatic reconstruction of spring-summer precipitation from the lower Bavarian Forest region, Germany. Int. J. Climatol. 25 611–630. 10.1002/joc.1150 DOI

Wirth C., Schumacher J., Schulze E.-D. (2004). Generic biomass functions for Norway spruce in Central Europe–a meta-analysis approach toward prediction and uncertainty estimation. Tree Physiol. 24 121–139. 10.1093/treephys/24.2.121 PubMed DOI