Environ. Sci. Technol. 2007, 41, 5778-5782
Carbon Isotopes in Tree Rings of Norway Spruce Exposed to Atmospheric Pollution H A N A Sˇ A N T R U ° C ˇ K O V AÄ , * , † J I Rˇ IÄ Sˇ A N T R U ° C ˇ E K , † , | J I Rˇ IÄ Sˇ E T L IÄ K , † MIROSLAV SVOBODA,§ AND J I Rˇ IÄ K O P AÄ C ˇ E K †,‡ Faculty of Science, University of South Bohemia, Branisˇovska´ 31, 37005 C ˇ eske´ Budeˇjovice, Czech Republic, Hydrobiological Institute, Biology Centrum of Academy of Sciences of The Czech Republic, 37005 C ˇ eske´ Budeˇjovice, Czech Republic, Faculty of Forestry and Environment, Czech Agriculture University, Kamy´cka´ 7, 165 00 Prague, Czech Republic, and Institute of Plant Molecular Biology, Biology Centrum of Academy of Sciences of The Czech Republic, 37005 C ˇ eske´ Budeˇjovice, Czech Republic
The Bohemian Forest was exposed to high levels of sulfur and nitrogen deposition during the last century. The change in acid deposition caused a rapid decline in pH and increase in Al concentrations of soil solutions since the 1950s. A possible negative effect of soil chemistry on growth of Norway spruce tree has been studied using the 13C isotopic signal and chemistry of the tree rings. Tree rings were sectioned by decades, and whole wood was analyzed for isotopic composition (∆ 13C) and content of Mg, Ca, and Al. Only those rings that formed after the juvenile effect in early rings were used and trends from the beginning of 20th century were evaluated. The mean ∆ 13C of the spruce tree rings was 17.6%. The ∆ 13C did not follow climate changes but had an opposite trend to that of acid depositions and Al concentrations in soil solution, but a similar trend as soil acidification (pH decrease), implying a negative effect of acid deposition and soil acidification on tree physiology. The molar ratio of base cations to Al decreased together with ∆ 13C.
Introduction European mountain ecosystems have been exposed to continuously increasing sulfur and nitrogen deposition over more than one century (1). Even though acid deposition has decreased since the 1980s, forests in acid sensitive areas, usually in those with crystalline bedrock and naturally a low base saturation of soils, remained exposed to the effect of soil acidification accelerated by atmospheric depositions. In addition to atmospheric acid inputs, soil acidification was historically amplified by frequent forest harvesting and the natural acidifying effect of spruce monocultures planted in central Europe during the last two centuries (2, 3). The present * Corresponding author e-mail:
[email protected]; phone: +420 387 772 361; fax: +420 387 772 359. † Faculty of Science, University of South Bohemia. ‡ Hydrobiological Institute, Biology Centrum of Academy of Sciences of The Czech Republic. § Faculty of Forestry and Environment, Czech Agriculture University. | Institute of Plant Molecular Biology, Biology Centrum of Academy of Sciences of The Czech Republic. 5778
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spruce forest decline with typical syndromes of needle loss and chlorosis is indisputable (2), but the prediction of future impacts based on scenarios of atmospheric pollution and climatic changes urgently needs information regarding when and under which environmental conditions tree damage has occurred. The combination of long-term records of climate, soil chemistry, and tree health could provide a powerful tool to unravel the historical status and predict the fate of future vegetation development in the impacted areas. The historical vegetation status can be derived through changes in tree ring composition. The chemical composition of tree rings records the availability of aluminum (Al) and base cations in soil solutions at the time of their formation and archives the historical development of adverse effects on tree health in the ecosystem (4, 5). In addition to the metal chemistry, the isotopic composition of the tree rings, δ 13C, represents a useful diagnostic tool, reflecting tree physiology (e.g., refs 6 and 7; for more details see Supporting Information). Tree physiology, growth, and 13C discrimination have been affected by the increasing concentration of atmospheric CO2, temperature and precipitation changes, nitrogen and sulfur deposition, and air pollution during the last century (6, 8-10). The effects of temperature, increasing CO2, irradiance, and humidity or water availability on 13C discrimination and growth have been well documented (1114), but less is known about the effect of soil chemistry (15, 16). As far as we are aware, almost no results relating the 13C isotopic composition of tree rings to soil chemistry have been published. The lack of information is caused by scarcity of long-term data series on soil chemistry interpretable for the study of ecosystems and deficiency of having both soil chemical and dendrochemical data for the same site. The development of long-term trends in soil solution chemistry can be, however, reasonably reconstructed and predicted by process-based models, such as, for example, MAGIC (modeling the acidification of groundwater in catchments, 17, 18; for details see Supporting Information). In this study, the results of tree ring analyses were related to the reconstructed chemical trends in sulfur emissions and soil water composition and the climate record with the aim of determining if long-term effects of sulfur emissions, soil acidification, and climate change on spruce tree physiology can be recorded by the isotopic and chemical composition of tree rings. Two watersheds in the Bohemian Forest (southwestern part of the Czech Republic), vegetated by a seminatural ∼150-year old spruce forest, exposed to heavy N and S deposition since the 1950s (19), and exhibiting a significant increase in annual air temperature (by ∼1.5 °C since the 1960s, 20) have been used as a model area.
Materials and Methods Site Description. The trees analyzed were sampled in the Plesˇne´ and C ˇ ertovo Lake watersheds in the Bohemian Forest, Czech Republic. The watersheds are situated between 48°47′ and 49°11′ N, and 13°52′ and 13°12′ E, at elevations from 1008 to 1378 m above sea level. Both watersheds have been exposed to heavy atmospheric pollution during the last century (Figure 1a). The acid deposition since the 1950s caused significant changes in soil chemistry and high nutrient leaching from the soils (19). The effect of acidification was boosted by spruce monocultures that were used to replace the natural mixed forest in the 19th century. Currently, the soils are N-saturated and have acidic leptosol, podzol, and spodo-dystric cambisol, with low (150 years old, were sampled in both the C ˇ ertovo (2 samples, elevations of 1290 and 1080 m) and Plesˇne´ (one sample, elevation of 1316 m) watersheds. Healthy trees, growing on places representative in slope, exposition, soil, and moisture conditions, were selected for the sampling. The disks were cut from near breast height and sectioned by decades to blocks; each block included late wood at one end and with early wood at the other end. For each decade, blocks from two opposite radii in the south to the north orientation were pooled together. Samples were dried at 60 °C, homogenized in a ball mill (MM200 Retsch, Haan, Germany), and used for chemical and ∆ 13C analyses. An important assumption of chemical and isotopic analyses of tree rings to provide a retrospective insight into changes in tree physiological processes is that the wood component being analyzed was not modified after wood formation (8). In the present study, not just one component but the whole wood was analyzed. It is well documented that whole wood can reliably be used instead of cellulose and produces the same trend (24, 53, 48). The total concentration of metals (Ca, Mg, and Al) was analyzed from H2SO4, HNO3, and HF mixed-acid digest (200 °C, 2 h) by flame atomic absorption spectrometry. Ca is an adequate marker of environmental changes because its translocation is apoplastic. Mg is translocated through active transport in the symplast, as well as the apoplast. Hence, Mg is probably of less indicative value, but tree ring enrichment, which might be interpreted as a signal of increased availability of Mg, has been shown (5, 31). Ratios of the molar concentration of Ca/Al have been useful markers of environmental stress, mainly, in root tips and in the wood (31, 49); the Ca/Al ratio in wood concurrently decreased with increasing sulfur emission (25). Norway spruce is ideal for dendrochemistry because its heartwood has an irreversible nature (25), and the heartwood/ sapwood Ca concentration ratio is close to 1 (1.17, 42). The isotopic composition of carbon (δ 13C) was determined using an elemental analyzer (EA1110, ThermoQuest, Italy) linked to DeltaXLplus (ThermoFinnigan, Bremen, Germany). The 13C concentrations were recalculated versus the VPDB (Vienna-Pee Dee Belemnite) standard. The isotope ratios were expressed in terms of discrimination against 13C in the atmosphere (∆ 13C, Farquhar et al., 1989) to remove an effect of atmospheric δ 13C decline. The atmospheric δ 13C signal was corrected using the Antarctic ice core record according to ref 6. The ecophysiological effect of differences in isotopic
TABLE 1. Soil Chemical Properties of Soil in the Cˇ ertovo and Plesˇ ne´ Watershedsa total content (mol kg-1)
exchangeable cations (mmolC kg-1)
extractable cations (mmol kg-1)
pH
watershed
C
N
P
Ca2+
Mg2+
Na+
K+
Al3+
H+
SRPox
Alox
Fecd
H2O
CaCl2
C ˇ ertovo Lake Plesˇ ne´ Lake
6.0 10.1
0.26 0.42
0.024 0.020
4.6 11.4
1.9 2.9
1.0 2.8
2.2 2.5
65 73
29 35
8.0 6.9
145 158
350 83
4.0 3.8
3.5 3.1
a The numbers represent the watershed weighed means obtained by weighing the soil parameters by their spatial coverage in the watershed. Total C and N concentrations were determined by CN analyzer, and total P was determined by HNO3 and HClO4 digestion. Exchangeable base cations (Ca2+, Mg2+, Na+, and K+) and exchangeable acidity (Al3+ and H+) were determined by extraction with NH4Cl and KCl, respectively. Extractable cations were measured in oxalate (Alox; soluble reactive P, SRPox) and citrate dithionite (Fecd) extracts. Soil pH is shown for water and CaCl2 extracts. For more details, see refs 21, 22, and 47.
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FIGURE 3. Mean air temperature and precipitation to evaporation ratio (P/E ratio; 23) during the vegetation season from May to September. The upper bold line represents 10-year moving averages of temperature; the upper thin line represents the long-term mean temperature from the 1885-2003 period; the lower bold line represents 10 year moving averages of P/E ratio; the lower thin line represents the mean P/E ratio from 1961-2003. Mg/Al) in the wood decreased over time in accordance with the Ca/Al and Mg/Al ratios in the soil solution (Figure 2, for more detail see Supporting Information).
Discussion FIGURE 2. Molar ratio of calcium to aluminum (Ca/Al) and magnesium to aluminum (Mg/Al) in soil solution and 10-year tree ring samples of three spruce trees over the 1880-2000 period. Molar ratios in soil solution were reconstructed by a MAGIC 7 model (19), and each point of the molar ratio in the tree rings represents the average from three trees (details see in Supporting Information, Figure 1). composition of early and latewood (54) was not considered in our conditions (for details see Supporting Information). To remove a possible juvenile (or age) effect (26, 27), only those tree rings that formed after any juvenile effect had ceased (older than 40 years) were included in the analysis. The record from 1874 to 2002 was then evaluated for ∆ 13C in all trees.
Results Environmental Conditions. Acid deposition significantly affected the Bohemian Forest soil chemistry. Soil water pH decreased sharply until the 1980s after a slow decline between 1850 and 1950 (Figure 1b). As a result, Al concentrations in the soil solutions increased (Figure 1a), and the Ca/Al and Mg/Al ratios decreased (Figure 2). These trends reversed in the 1990s because of decreasing atmospheric acidification (Figures 1a and 2), and soil water chemistry began to recover. Mean air temperature during the vegetation season (May to September) was 10.1 °C during the 1781-2002 period, and the decadal averages have increased above the mean value since the late 1960s (Figure 3). The P/E (precipitation to evaporation) ratio was >0.8, and its decadal averages decreased over the recorded period (Figure 3). Tree Ring Isotopic Signal and Chemistry. The ∆ 13C of the tree rings did not change significantly from 1874 until the late 1940s, decreased to a minimum of 15.7% in the late 1970s and 1980s, and then increased slightly in the 1990s (Figure 1b). The mean ∆ 13C for the whole period was 17.4 ( 1%, with ∆ 13C values falling below the mean in the 1960s, corresponding to the rapid decreases in soil pH and molar Al/Ca ratio and increased Al concentrations and acid deposition (Figures 1 and 2). The trend of ∆ 13C changes closely paralleled soil pH and Ca/Al and was opposite to that of soil Al concentration and acid deposition. ∆ 13C did not correspond to a similar extent with mean air temperature and P/E ratio. The molar ratios of Ca or Mg to Al (Ca/Al, 5780
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Our observations of 13C discrimination imply that spruce tree physiology was affected by pollutants more than by increasing temperature in the Bohemian Forest. But several factors usually control variability in ∆ 13C, and interpretation of correlations with a single parameter deserves a caution (6). Even if the relation is significant, it does not imply that the checked factor per se controlled the isotopic signal. The environmental factors controlling ∆ 13C in temperate conditions can switch from one to another, reflecting their actual growth limiting impacts during the vegetation period (8). Only a weak relationship was observed between ∆ 13C and mean air temperature or P/E ratio during the vegetation period. The P/E ratio characterizing water availability was higher than 0.8, suggesting a low probability of drought stress and dominance of other influences (10). The effect of low water availability, however, cannot be excluded. In the studied area, Al and NO3 concentrations were high, causing trees to develop shallow root systems mainly in organic horizons (28-30). The upper soil horizons can dry out on warm summer days, even if the average P/E ratio of the area is high. Consequently, we hypothesize that the effect of increasing temperature could contribute to the major chemical stress of spruce trees, especially during the last two decades. ∆ 13C decreased below the average value in the 1960s, indicating that reduction in CO2 availability in the chloroplasts (ci/ca decrease) occurred. ∆ 13C concurrently decreased with increased sulfur emissions and soil Al concentrations, but decreased pH, which indicates an adverse effect of air pollution or soil chemistry on photosynthetic CO2 fixation. The ultimate result of impaired photosynthetic performance, that is, slow growth and decreased wood productivity, should follow the shift in isotopic signal (9). No parameter of wood productivity was measured in this study, but the growth depression of Norway spruce was detected in the Bavarian Forest (50) and the northern part of the Czech Republic (51) on sites with acid bedrock and a similar pollution history in the identical period. Sulfur dioxide emissions can play a part in the observed trend in ∆13C alteration of the stomatal function in damaged spruce needles. Varying stomatal conductance should bring a shift in ∆13C and, indeed, decreased ∆13C in tree rings in areas adjacent to smelters has been reported (9, 45). However, Schulze et al. (44) found no difference in isotopic signal of
spruce needles between healthy, unpolluted and declining, polluted sites in Germany. Evidence exists that acid depositions may deplete available base cation pools and increase Al toxicity in soils to the extent that the tree growth may be reduced (32). Even though soil pH was positively related to ∆13C, it is most likely that pH per se did not affect ∆13C. Soil pH decreased only by about 0.6 units (from ∼4.6 to ∼4.0; Figure 1). Such a decrease could significantly affect availability and activity of chemical elements, but the harmful influence on spruce trees is not probable. In contrast, Al mobilized under low-pH conditions can affect tree physiology because of Al toxicity of fine roots (33, 34). The litter layer of the Bohemian Forest watersheds contained much more Al than the litter layer of spruce forests in Northern Europe (35, 36), indicating more available for enhanced consumption of Al by vegetation in the Bohemian Forest watersheds. In the Bohemian Forest soils, the amount of exchangeable Al3+ exceeded ∼20 mmol kg-1, making it possible that there would be a toxic effect of Al on plant growth (37, 38). This suggestion is supported by the 5-10 times higher Al concentrations in 1-3 year-old spruce needles in the Bohemian Forest than that in similar Northern European samples (35). Al also interferes with the uptake of base cations by fine roots. The impaired base cation uptake magnified the negative effect of base cation deficiency on tree health in acidified soils (32, 39). Base cation shortage and Al mobility is obviously indicated by the reduced Ca/Al and Mg/Al ratios in the soil, needles, fine roots, and wood (40-43). The molar Ca/Al ratio of the studied tree rings declined from 30 to 70 in the 19th century (Figure 2) to the current 20-30, and the Mg/Al ratio decline followed a similar pattern. The MAGIC model showed that the molar Ca/Al ratio in soil solutions decreased from 1 to 0.7 and 0.3 in the Plesˇne´ and C ˇ ertovo soils, respectively, between the early 1900s and 2000 (19). One would expect a difference in the ∆ 13C or Ca/Al ratio in tree rings between watersheds. It was not the case in this study, and we speculate that trees growing for more than 100 years at the sites might acclimate to permanently low base cation to Al ratios. Only when the Ca/Al ratio decreased under the long-term value, did the trees respond. On the basis of an extensive review of available data, Cronan and Grigal (41) estimated the risk of soil Al stress and subsequent growth impact when the Ca/Al ratio of soil is below 1. The MAGIC model showed slow recovery of soil conditions from the early 1990s. MAGIC data are in agreement with the real soil solution data measured by Pannatier et al. (52) at a site with similar deposition in the upper layers under the litter layer. The real solution data indicate that the recovery of the mineral horizons is much slower. Base cation/Al ratios start to recover and acidification slows, first in the upper layers and then in the deeper layers. The recovery of the upper layers is of main importance for spruce trees, the rooting zone of which is mainly in the upper organic horizons (28-30). There is a proportional relation between ∆ 13C in tree rings as an indicator of physiological activity and soil pollution. Both of these parameters respond quickly to a reduction in atmospheric deposition. By contrast, ratios between base cations and Al in the soil solution and in the tree rings both continue to decline for at least a decade despite reduced atmospheric deposition. This may also mean that base cation to Al ratios in soil solution are not really a sensitive indicator of tree health but might show only root functioning conditions.
Acknowledgments This study was supported by Projects GA CR 206/07/1200, GA AS A601410505, MSM 6007665801, and CZ 0051 (01-04/ 05-081 IP-65 MZP). We acknowledge the laboratory and field
assistance provided by our colleagues and students. We also thank Keith Edwards for language corrections and the authorities of NP Sˇ umava for its permission to study the lake ecosystems.
Supporting Information Available More detailed descriptions about the site, background information of 13C discrimination in plants and MAGIC model calibration (Table S1 of model parameters), and details of base cation to Al ratios in Figure S1. This material is available free of charge via the Internet at http://pubs.acs.org.
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Received for review January 3, 2007. Revised manuscript received May 25, 2007. Accepted June 8, 2007. ES070011T
