Tree and stand growth of mature Norway spruce and European beech under long-term ozone fumigation

Environmental Pollution 158 (2010) 1061–1070

Contents lists available at ScienceDirect

Environmental Pollution journal homepage: www.elsevier.com/locate/envpol

Tree and stand growth of mature Norway spruce and European beech under long-term ozone fumigation Hans Pretzsch a, *, Jochen Dieler a, Rainer Matyssek b, Philip Wipfler a a b

¨ t Mu ¨ nchen, Am Hochanger 13, D-85354 Freising, Germany Chair for Forest Growth and Yield Science, Technische Universita ¨t Mu ¨ nchen, Am Hochanger 13, D-85354 Freising, Germany Chair for Ecophysiology of Plants, Technische Universita

Ozone effects on tree growth and stem shape were investigated for Norway spruce and European beech; the study reveals species-specific reaction patterns in growth rate and allometry under ozone exposure.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 July 2009 Accepted 26 July 2009

In a 50- to 70-year-old mixed stand of Norway spruce (Picea abies (L.) Karst.) and European beech (Fagus sylvatica L.) in Germany, tree cohorts have been exposed to double ambient ozone (2O3) from 2000 through 2007 and can be compared with trees in the same stand under the ambient ozone regime (1O3). Annual diameter growth, allocation pattern, stem form, and stem volume were quantified at the individual tree and stand level. Ozone fumigation induced a shift in the resource allocation into height growth at the expense of diameter growth. This change in allometry leads to rather cone-shaped stem forms and reduced stem stability in the case of spruce, and even neiloidal stem shapes in the case of beech. Neglect of such ozone-induced changes in stem shape may lead to a flawed estimation of volume growth. On the stand level, 2O3 caused, on average, a decrease of 10.2 m3 ha1 yr1 in European beech. Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: Free-air ozone fumigation Stress response Shoot allometry Stem form factor Tree height growth Stem diameter growth Volume growth

1. Introduction High ozone regimes – resulting from industry and traffic – have spread across major urban areas of the world and even to rural regions. Towards the beginning of the 21st century, this photooxidant has become a pollutant of great concern (Ashmore, 2005; Sitch et al., 2007; Vingarzan, 2004). Tropospheric ozone levels increased by factor two during the past century (Stockwell et al., 1997; Volz and Kley, 1988). Peak concentrations are declining whilst the background ozone concentration is steadily increasing (Jonson et al., 2006; Penkett, 1988). If the global emission trends continue, ozone levels will rise by another 50% by the end of this century (Meehl et al., 2007). The enhanced O3 regimes will impact the vegetation and may reduce forest productivity (Matyssek and Innes, 1999; Ska¨rby et al., 1998; Taylor et al., 1994) causing yield losses of considerable economical importance (Ashmore, 2005; King et al., 2005; Morgan et al., 2006). In addition to the direct growth reduction, ozone can induce long-term effects of practical importance like the alteration of the competitive situations in mixed stands

* Corresponding author. Tel.: þ49 8161 714710; fax: þ49 8161 714721. E-mail address: [email protected] (H. Pretzsch). URL: http://www.wwk.forst.tu-muenchen.de 0269-7491/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2009.07.035

(Karnosky et al., 2005) leading to stand compositions which differ from forest planning and required silvicultural interventions. Many studies focused explicitly on ozone effects within plants (Dizengremel, 2001; Clark et al., 2000; Nunn et al., 2005a), other studies use ozone as a stress factor to analyze the defense reaction of plants in general (Sandermann et al., 1998). Although evaluations dealing with chemical, physiological, and anatomical effects of ozone on trees (e.g. leaf injuries) are well known (Matyssek and Sandermann, 2003), only fragmentary assessments exist about ozone effects on the productivity of mature forest trees and stands (Matyssek and Innes, 1999; Matyssek et al., 2007). Results about the behavior of herbaceous plants and young trees have often been obtained by performing ozone exposure experiments in phytotrons or open-top chambers (Broadmeadow et al., 1999; Clark et al., 2000; Dixon et al., 1998; Liu et al., 2004; Maurer and Matyssek, 1997). However, the results can hardly be transferred to mature trees or even stands under natural conditions (Kolb and Matyssek, 2001; Nunn et al., 2005b). Nonetheless, a few results from field studies on adult trees are available. Wipfler et al. (2005) found a decline in diameter growth at breast height of about 20% on ca. 50-year-old spruce trees, whereas the diameter growth of ca. 60-year-old beech trees remained unaffected. Karlsson et al. (2006) reported on decline in basal area increment of 4.6% in 19- to 35-years-old Norway spruce at the tree level, and Braun et al. (2007) on a decrease of height

1062

H. Pretzsch et al. / Environmental Pollution 158 (2010) 1061–1070

growth by 4.7% in 60- to 180-year-old beech stands. Studies on black cherry and yellow poplar revealed O3-induced stem radial growth losses by 8–12% and 30–43%, respectively (Somers et al., 1998). Vollenweider et al. (2003) derived stem radial growth losses of 28% from a long-term study on black cherry. Yet, such growth losses are either not applied to the whole tree or they are up-scaled to the tree and stand level via modeling (Laurence et al., 2001), often based on unclear assumptions about alterations of stem shape and shift of form factor (Deckmyn et al., 2007). Hence, knowledge about the differential response of tree organs and dimensions to ozone, which is the ultimate expression of resource allocation at the whole-plant level under stress impact and, hence, a pre-requisite for understanding both ecological performance and economic yield, is still missing (Matyssek et al., 2005). Some further answers may be provided by the large-scale ozone fumigation experiment ‘‘Kranzberger Forst’’ near Freising in southern Bavaria, which started in 2000 and provides 8 years of data. The experiment was conducted on mature trees of Norway spruce (Picea abies (L.) Karst.) and European beech (Fagus sylvatica L.) in a mixed stand under natural growing conditions, whose reaction to ozone fumigation is poorly understood. Previous studies were focused either on diameter or height development (Matyssek et al., 1993, 2007; Wipfler et al., 2005). Alterations in stem form and changes in productivity on stand level which are highly relevant for forest practice had not been considered. Here, besides changes in diameter and height, also changes in the stem form have been recorded precisely and are compared to adjacent non-fumigated trees of the same stand. By using the increment trend method (Deutscher Verband Forstlicher Forschungsanstalten, 1988; Pretzsch, 2009) initial growth differences between the target and reference collectives can be eliminated. This method allows for accurate quantification of tree growth reaction and exact quantification of the loss of volume growth. Overall, this study focuses on the three following questions: Q1: Does the annual diameter increment of Norway spruce and European beech trees after 8 years of 2O3 exposure differ from trees under the unchanged 1O3 regime prevailing at the site? Q2: Does long-term 2O3 exposure alter the height–diameter allometry of the stems of Norway spruce and European beech? Q3: Do the mean periodic increments of diameter, basal area, height, the change of the form factor, and the resulting volume show response to enhanced ozone exposure? In a first report after only three years of ozone exposure, we found a 22% decrease of radial stem increment for Norway spruce while European beech showed no change on the basis of successive stem diameter measurements (Wipfler et al., 2005). This report, in contrast, reveals long-term effects after 8 years of ozone exposure on the basis of tree ring analysis, height increment measurements and retrospective analysis of stem form development. 2. Material and methods 2.1. Stand and sample tree characteristics The experimental plot ‘‘Kranzberger Forst’’ is under survey since 1994 and is located at 11390 4200 E, 48 2501200 N in the ecological region 12.8 ‘‘Tertia¨res Hu¨gelland. Oberbayerisches Tertia¨rhu¨gelland’’ in southern Bavaria near Freising, 35 km northeast of Munich. The altitude is 490 m above sea level. The research plot has a rectangular shape of 50100 m. Mean annual temperature is 7.0–7.5  C and precipitation 730–890 mm per annum. The corresponding temperature and rainfall during the vegetation period are 14.0–15.0  C and 410–520 mm, respectively. The prevailing soil is parabrown soil, based on loess and tends to pseudo-gley. The potential natural vegetation is a Galio-odorati-Fagetum association, dominated by European beech (Pretzsch and Schu¨tze, 2009). The experimental design comprises pure stands of Norway spruce and European beech and in-between a stand section in which both species are mixed as individual

trees or clusters. The ozone fumigation experiment was established in the mixed zone of the stand. The ages of the spruce and beech trees were determined as 56 2 and 66 4 years, respectively, in 2007. The characteristics of the stands are summarized in Table 1 which reflects the growing conditions from the beginning through the end of the analyzed period and refers to the neighboring pure stands of Norway spruce and European beech each under the ambient ozone regime. As no thinning measures were carried out since 10–20 years before the first survey in 1994, the reduction in stem number between 1994 and 2007 is solely due to selfthinning. 2.1.1. Ozone fumigation within the stand Within the mixed stand zone of the experimental plot ‘‘Kranzberger Forst’’ the ozone fumigation experiment was initiated in 2000. It covers one of the groups of beech trees together with neighboring spruces, comprising the most intensively studied section of the experimental site (Pretzsch et al., 1998). This part of the stand is growing under self-thinning conditions and was fumigated with ozone by means of ‘Kranzberg Ozone Fumigation Experiment’ (KROFEX), representing a free-air methodology of O3 release (Karnosky et al., 2007; Nunn et al., 2002; Werner and Fabian, 2002) from spring 2000 through fall 2007. Five neighboring beech and spruce trees were experimentally exposed to a fluctuating double ambient ozone regime (2O3), allowing O3 levels of 150 nl l1 at maximum to prevent acute O3 injury. A corresponding group of trees growing under the unchanged ambient air at the forest site (1O3) served as control. Due to the prevailing west winds, the unfumigated trees are located upwind. O3 levels generated by 2O3 were within the range of those occurring under unchanged forest conditions, although the enhanced frequency of the experimental O3 levels warranted a chronically elevated O3 exposure (Matyssek et al., 2007). The 2O3 regime was maintained during the growing season of each year (April through November), defined as the time span between flush and autumnal shedding of leaves in beech. In this way, the achieved experimental period of 8 consecutive years was unprecedented for studying the response of adult forest trees to a controlled, elevated O3 regime under stand conditions. 2.1.2. Measurements at tree and stand level At the date of the plot establishment in autumn 1994, the precise positions of all trees were determined by theodolite (LEICA TC500); diameter at breast height was documented by girth tapes; and tree and crown heights were measured with ¨ F VERTEX). Since 1999, measurements of the diamultrasonic hypsometer (HAGLO eter at breast height are available for all trees in the stand. Based on permanent girth tapes, the values were read by monthly intervals during the vegetation period. Due to the permanent installation and the additional vernier scale, these tapes allow measurements of an accuracy of 1 mm. The differences of the January value of two successive years are defined as annual diameter growth. Measurements of tree height and crown height were re-measured in 1994, 1999, 2002 and 2007 on sample trees. These data were used to construct height–diameter curves to estimate the height of all trees. 2.1.3. Sample trees In contrast to previous reports (Nunn et al., 2005a; Matyssek et al., 2007; Wipfler et al., 2005) about ozone effects on tree and stand growth in Kranzberg, this study includes the complete 8-years time series of the ozone fumigation. This study is based on the diameter and height measurements at the survey times (1994, 1999, 2007) and additional increment cores from a selected set of fumigated trees and non-fumigated trees. To guarantee comparability of the data, the sampled trees all possessed a dominant or co-dominant position within the stand. The increment cores additionally allow an annual resolution of growth differences. For the evaluation of questions Q1–Q3, we selected two different samples (Table 2) due to different demands on data resolution and precision. The sample for Q1 and Q3 consists of 11 spruces and 10 beeches: 6 reference spruce and 5 reference beech trees (1O3), and 5 spruce and 5 beech trees under double ambient ozone (2O3). Aside from basic yield measurements, such as diameter at breast height or tree height, stem diameter was also measured at a height of 0.6 m as well as in 50 and 70% of tree height from a crane. At every tree height, breast height included, increment cores were taken in order to trace back increment and stem shape development (Fig. 1b). Increment data are available back to the pith. This allows on the one hand an annual resolution of the diameter development (Q1) and on the other hand very precise determination of the (periodic) form factor and volume development (Q3). The sample for analyzing the height–diameter allometry (Q2) consists of 11 spruces and 7 beeches under ambient ozone and 11 spruces and 6 beeches under double ambient ozone, respectively. Height and diameter were measured in 1994, 1999, and 2007 (Fig. 1a). This sample includes the Q1/Q3 trees in the experiment and other trees for which passive ozone samplers indicated similarly high ozone levels during the 8 years of fumigation. Fig. 1a displays the measurements for detecting changes in the height–diameter allometry, and Fig. 1b the measurement of diameter and sampling of increment cores in various tree heights in order to reveal any changes of the form factor (f) of the stem by long-term ozone fumigation. The two non-fumigated pure stands of Norway spruce and European beech (Table 1) provide the basis to assess the change in yield on stand level under double ambient ozone. Both stands are far enough away and unaffected by the ozone

H. Pretzsch et al. / Environmental Pollution 158 (2010) 1061–1070

1063

Table 1 Growth and yield characteristics of the two sampled pure stands of Norway spruce and European beech. Stand variables refer to autumn 1994, 1999, and 2007, periodical annual increment refers to the 5-year period 1995–1999 and to the 8-year period 2000–2007. Volume is given as merchantable wood above 7 cm in diameter at the smaller end. Stand

Survey

Age (yr)

Numbers trees (trees ha1)

Stem diameter (cm)

Tree height (m)

Basal area (m2 ha1)

Standing volume (m3 ha1)

Periodic annual increment (m3 ha1 yr1)

Norway spruce

1994 1999 2007

53 58 66

1218 861 758

23.8 27.7 30.7

23.2 24.9 27.8

40.4 48.3 60.0

478.6 606.8 826.1

26.4 27.3

European beech

1994 1999 2007

43 48 56

1503 1343 1051

18.9 22.1 24.0

22.5 24.5 27.5

41.6 44.1 52.4

472.2 552.2 740.3

18.4 23.5

exposure but close enough to serve as reference stands (Pretzsch et al., 1998; Pretzsch and Schu¨tze, 2005). 2.2. Evaluation methods 2.2.1. Detection of annual diameter losses by the increment trend method (Q1) The increment trend method was developed to estimate increment losses of forest trees which have been affected by forest dieback in the 1980s (Pretzsch, 2009). The damaged trees’ increment curves were compared to those of healthy trees on the same plots. Hence, this method uses healthy individuals in the same stand as a reference. This has the advantage that similar site fertility can be assumed for the group of reference and disturbed trees. Nevertheless, one must ensure that the growth level and canopy position of the damaged and reference trees are comparable before the damage. In the first step, the diameter increment time series of the non-fumigated tree group (denoted R1.Rn, n ¼ number of trees) and fumigated trees (denoted A1.An) are used to calculate the mean diameter growth r j and aj for each group and year j (j ¼ 1.m, m ¼ number of the years). In our case n ¼ number of sample trees and m ¼ number of years from 1994 to 2007. This first step yields the two mean curves R for the reference group and A for the trees to be assessed. Based on those curves, the second step compensates for differences in the increment level that might already have existed before the onset of the disturbance. The onset of the disturbance was in 2000 when the O3 fumigation of parts of the stand began. Hence, the preceding period 1994–1999 without ozone fumigation serves as a reference period and the mean annual increment in this period r refper and arefper is calculated for both groups. In the next step, this mean increment rrefper respectively arefper in the reference period is set to 100% and the whole increment curve is referenced to these group means in the reference period. This first percentage serves to eliminate the offset between both groups before onset of the disturbance and results in the percentage curves R% and A% . In the next step the A% time series ða%j;j¼1.m Þ is set in relation to the reference time series R% ðr %j;j¼1.m Þ in order to quantify the increment losses (Equation (1))

loss idj ¼

1

a%j r%j

!  100

(1)

where loss idj is the diameter increment loss (in percent) of the fumigated trees in year (j) compared to the reference trees in the same year (second percentage). Analogously, the method can be applied to estimate basal area loss iba, height loss ih or volume increment loss iv. This calculation is executed for each year to get a time series of annual increment losses for the group of damaged trees for all m years in the period j ¼ 1.m. In essence, the increment trend method first eliminates initial differences between the two groups and then sets the growth of the damaged trees in relation to the reference group in order to get increment losses unflawed by initial differences. The increment trend method conforms to the recommendations of the Forest and

Yield Science Section of the German Union of Forest Research Organizations (Deutscher Verband Forstlicher Forschungsanstalten, 1988) for increment diagnoses in damaged forest stands. 2.2.2. Detection of changes in height–diameter allometry (Q2) To assess whether doubling of the ambient ozone concentration affects the proportion between growth of stem diameter and height we determine the allometric exponent:

bh;d ¼

lnðhiþ1 Þ  lnðhi Þ lnðhiþ1 =hi Þ ¼ lnðdiþ1 Þ  lnðdi Þ lnðdiþ1 =di Þ

(2)

The value pairs hi, hiþ1 and di, diþ1 represent the tree height and the tree diameter (d1.3 ¼ diameter at breast height) measurements, respectively, from consecutive surveys of the ambient (1O3) and double ambient (2O3) sample trees (Table 2). Exponent bh;d comes from allometrical theory (Pretzsch, 2006) and describes the relationship between the relative growth rate of an individual’s organ (y) and the relative growth rate of another organ (x) (or of the entire body): dy=y ¼ by;x dx=x

(3)

with dy, dx ¼ increment, y, x ¼ body size of y and x, and bx;y ¼ allometric exponent. The reason for calling bh;d allometric exponent is that the integral of Equation (3) reads y ¼ axby;x , where a is the integration constant. When plotted on a ln–ln scale, b becomes the slope of a linear equation: lnðyÞ ¼ lnðaÞ þ by;x lnðxÞ which can be determined as in Equation (2). The physiological interpretation of Equation (3) is that the allocation of resources depends on the current size of the organs and bh;d present the distribution between organ (y) and (x) (Von Bertalanffy, 1951), e.g., if bx;y ¼ 1:5, a one-percent increase of (x) is coupled with a 1.5-percent increase of (y). Accordingly, the ratio bh;d ¼ lnðh2 =h1 Þ=lnðd2 =d1 Þ reflects a tree’s allocation of resources into height vs. diameter. The higher bh;d is, the more pronounced is the trend to expand vertically instead of laterally. We use it to quantify the period-wise proportion of matter allocation between (h) and (d) and to reveal any differences in 1O 2O the allometric exponents of 1O3 and 2O3 sample trees ðbh;d 3 and bh;d 3 Þ. 2.2.3. Detection of changes in the development of mean periodic diameter, basal area, height, false form factor and the resulting volume (Q3) For this question, it was necessary to quantify tree stem shape using the false form factor f (Prodan, 1951). f ¼

v ba  h

(4)

where (v) represents the stem volume, (ba) the basal area at breast height and (h) the tree height. The attribute ‘‘false’’ is used to express that this form factor is always

Table 2 Sample trees of Norway spruce and European beech under ambient and double ambient ozone. For each value, arithmetic mean and standard deviation are shown. The samples differ depending on the examined questions. The measurements refer to autumn 1999 and 2007 and span an 8-year period. Sample

Tree species

O3 treatment

Stem diameter (cm)

Tree height (m)

Stem diameter (cm)

Tree height (m)

Q1, Q3

Norway spruce

1 2 1 2

   

O3 O3 O3 O3

6 5 5 5

30.7 28.7 22.9 26.7

(6.7) (7.2) (3.5) (7.3)

26.0 25.8 24.0 24.6

(1.9) (1.9) (0.7) (0.6)

33.1 30.1 25.1 28.1

(7.5) (7.6) (4.5) (8.2)

27.6 27.5 25.7 25.9

(2.1) (2.3) (1.5) (1.5)

1 2 1 2

   

O3 O3 O3 O3

11 11 7 6

30.9 28.6 25.9 27.1

(4.2) (10.4) (7.9) (8.7)

26.7 24.7 24.0 24.1

(1.1) (3.4) (0.6) (1.0)

34.3 30.8 28.2 29.1

(4.7) (11.0) (8.6) (9.2)

28.1 27.1 25.5 25.4

(1.5) (3.7) (0.5) (1.0)

European beech Q2

Norway spruce European beech

Number of trees

1999

2007

1064

H. Pretzsch et al. / Environmental Pollution 158 (2010) 1061–1070

a

b

70%

50% h1

h2

1.3m 0.6m d1 d2 Fig. 1. Measurements for detecting changes of height–diameter allometry bh,d and form factor (f) of the stem by long-term ozone fumigation. (a) Tree diameter at breast height and height were measured twice before beginning (d1, h1) and after ending (d2, h2) of the double ambient ozone fumigation in 2000 and 2007, respectively. (b) In various tree heights increment cores reaching back to the pith were taken after ending of ozone fumigation in 2007. referenced to diameter at 1.30 m height, rather than using a relative reference height which would yield the so-called true form factor. The form factor (f) expresses the share of the cylinder described by (ba) and (h), which is filled by the tree stem and is, therefore, an expression of the stem shape (Fig. 2). We used the diameter measurements and increment cores at different tree heights (Fig. 1b) to determine the current and past tree volume for the years 1994, 1999 and 2007. In order to consider the development of the bark in this period, we applied bark functions (Prodan, 1951), and the height development was reconstructed from individual height measurements. This database allows an accurate calculation of stem volume (v) from the sum of the stem sections for the years of the sample periods. The stem sections were assumed to be truncated cones, in case of the upper stem section of a cone. When stem volume (v), basal area (ba) and height (h) are known, we can apply Equation (4) to get the form factor (f) for all individual trees in 1994, 1999, and 2007. Based on the tree height (h) at the beginning of the survey period (t1), which is characterized by diameter at breast height (d1), tree height (h1) and false form factor (f1), we calculated the stem volume (v1). The repeated measurement procedure of d2, h2, and f2 at the time t2 provides the calculation of stem volume v2 as well as diameter increment id, height increment ih, if in false form factor f and volume increment iv between the two successive surveys t1 and t2 by Equation (5). (5)

i v ¼ v 2  v1

Once form factor and volume were determined precisely, we applied the increment trend method analogously on periodic annual increment diameter pid, basal area piba, height pih, volume piv, and changes of the tree form factor pif in order to reveal any effects of ozone (Q3). In this case, the evaluation was based on the individual trees’ periodic annual increment of diameter pid (and piba, pih, piv, and pif analogously) in the years 1995–1999 and 2000–2007. We refer to the increments in the two periods as piba95–99 and piba00–07, respectively. Whether a tree belongs to the group of reference trees or ozone fumigated ones is indicated by adding 1O3 and 3 2O3, respectively. So, pi1O ba 00—07 refers to the periodic annual basal area increment of a reference tree in period 2000–2007. In a first step we set for each tree the annual increment in period 2000–2007 in 3 3 3 ¼ pi1O =pi1O relation to the annual increment in 1995–1999 ðrpi1O ba 00—07 ba 00—07 ba 95—99 3 3 3 and rpi2O ¼ pi2O =pi2O Þ, respectively, that will allow to eliminate ba 00—07 ba 00—07 ba 95—99 any a priori differences between the reference group and the fumigated trees. For 3 3 3 is set in relation to rpi1O in a second step: rrpi2O ¼ this, rpi2O ba 00—07 ba 00—07 ba 00—07 which yields the corrected relationship between growth of =rpi1O3 rpi2O3 ba 00—07

ba 00—07

3 ozone fumigated and reference trees. A rrpi2O ba 00—07 value of 0.8 would indicate, that after elimination of initial growth differences the growth rate of ozone fumigated

Fig. 2. Concept of the false form factor (f) which is applied for analysis of stem form changes. trees was 0.8 times (80%) of reference trees. These relations are calculated for all fumigated Norway spruces and European beeches so that for both species mean and 95% confidence interval can be calculated for testing whether mean CI overlaps 1.0 (¼100%, i.e., identical growth) or falls significantly below 1.0. In order to get the percentage of basal area increment differences, we calculate in 3 a third step loss piba ¼ ð1  rrpi2O ba 00—07  100Þ. In the same three steps, ozone effects on periodic annual increment of diameter, height, volume, and changes of the trees form factor were calculated as loss pid, loss pih, loss piv, and loss pif, respectively. 2.3. Statistical analysis and definitions For brevity, we have omitted ‘‘measured at 1.3 m above-ground’’ in case of diameter at breast height and add them only when other stem heights are considered. The data were characterized by standard descriptive statistics; when we report standard errors they are one-fold, the reported confidence intervals always represent 95% limits. When t-tests are applied we report just significant results on the p < 0.05 level. For all statistical analysis we applied the statistical software package SPSS 16.0. In this report the term growth (e.g., stem growth at breast height) is used as a synonym for increment. It is the common practice in forest growth and yield science to measure stem dimensions in autumn after end of the vegetation period (Pretzsch, 2009). So, if we refer to a year of measurement, the increment of the respective year is included (e.g., diameter in 2007 refers to the size in autumn 2007). Analogously, the diameter increment (id) in the year 2007 is calculated as id2007 ¼ d2007  d2006.

3. Results 3.1. Detection of annual diameter growth losses at the individual tree level (Q1) Fig. 3 shows the annual diameter increment of the non-fumigated (1O3) and fumigated trees (2O3) from 1995 through 2007; the vertical line marks the beginning of the ozone fumigation. During the period before the ozone fumigation (1995–1999) the 1O3 group showed a mean annual diameter increment of 0.50 cm

H. Pretzsch et al. / Environmental Pollution 158 (2010) 1061–1070

a

1065

b

Fig. 3. Mean annual diameter increment at breast height id (cm yr1) based on increment core analysis of (a) Norway spruce and (b) European beech under ambient (1O3) and double ambient (2O3) ozone exposure. The reference periods from 1994 to 1999 are marked as R ð1O3 Þ and A ð2 O3 Þ. The vertical dashed line serves as the starting date of the ozone fumigation.

yr1 (0.04, n ¼ 6) for Norway spruce and 0.33 cm yr1 (0.03, n ¼ 5) in European beech. In addition, the graph reveals that already before beginning the ozone fumigation, the annual diameter growth of the 2O3 group was lower than that of the 1O3 group. In this period the growth amounted to 0.33 cm yr1 (0.03, n ¼ 5) in spruce and 0.26 cm yr1 (0.03, n ¼ 5) in beech. In total, in the case of beech the growth in both groups was quite similar in 1995– 1999, whereas it differed a bit more in the case of spruce. Within the fumigation period 2000–2007, an age-related decline of diameter growth was revealed in Norway spruce and European beech. The mean annual increment of the 1O3 group declined to 0.31 cm yr1 (0.03, n ¼ 6) in spruce and 0.27 cm yr1 (0.03, n ¼ 5) in beech. Under 2O3, the decrease in diameter increment reached 0.19 cm yr1 (0.02, n ¼ 5) in the case of Norway spruce and 0.19 cm yr1 (0.02, n ¼ 5) in European beech. The results of the increment trend method are shown in Fig. 4, where the growth of the 1O3 group is drawn as the zero line and the growth of the 2O3 group is set in relation to this reference. The graph shows for most of the years negative increment values of the fumigated trees relative to the reference group. 2O3 leads to a mean annual loss in diameter increment at breast height of 11.36% (6.61, n ¼ 5) in Norway spruce and 11.51% (6.12, n ¼ 5) in European beech. The average negative impact is similar for beech and spruce. While a downward trend is apparent in both species,

a

significant deviation from the reference occurs in the case of spruce only in 2004 and in beech only in 2002. In summary, even after elimination of initial growth differences, both species show a decrease of diameter growth under 2O3 fumigation, with growth losses of 11% on average and occasional significant (p < 0.05) deviations from the reference group. 3.2. Tree height–diameter allometry bh,d with and without ozone fumigation (Q2) Fig. 5 shows the tree height–diameter trajectories during the period of 2000 through 2007 for Norway spruce (a) and European beech (b) in the double-logarithmic grid. The slope of both 1O3 and 2O3 trajectories, equivalent with the allometric exponent bh,d, range between bh,d ¼ 0.27–2.42 (mean bh,d ¼ 0.99) in Norway spruce and bh,d ¼ 0.14–1.91 (mean bh,d ¼ 0.83) in European beech. The graphical impression that trees growing under double ambient ozone have steeper slopes can be substantiated by analysis of their allometric exponent bh,d. We compared the bh,d-values of the sample trees under 1O3 and 2O3 which are growing in the same stand and are similar in tree size, tree age, and crown parameters (Table 2). 1O The comparison yields for Norway spruce bh;d 3 ¼ 0:73 ð0:11; 2O n ¼ 8Þ and bh;d 3 ¼ 1:18 ð0:17; n ¼ 11Þ and for European beech 2O 3 b1O ¼ 0:73 ð0:18; n ¼ 7Þ and bh;d 3 ¼ 0:94 ð0:27; n ¼ 6Þ. For h;d

b

Fig. 4. Deviation of diameter increment at breast height loss idy (%) under long-term exposition of doubled ambient ozone (2O3) from diameter increment of tress under ambient ozone (¼0%) for (a) Norway spruce and (b) European beech. The analysis is based on increment cores. The whiskers illustrate the 95% confidence intervals of the mean value.

1066

H. Pretzsch et al. / Environmental Pollution 158 (2010) 1061–1070

a

b

Fig. 5. Tree height–diameter allometry bh,d of (a) Norway spruce and (b) European beech in period 2000–2007 under ambient (1O3) and double ozone concentration (2O3) represented by thin (1O3) and bold lines (2O3), respectively. The straight lines represent the height–diameter allometry lnðhÞ ¼ lnðaÞ þ bh;d lnðdÞ expected for geometric scaling with bh,d ¼ 1.0 and intercepts ln(a) ¼ 1.0, 0.0 and þ1.0 and serve as reference.

each group arithmetic mean of bh,d, standard error and sample size is reported (mean, SE, n). A t-test yields a significant (p < 0.05) increase of height–diameter allometry under 2O3 in the case of Norway spruce and an insignificant increase of mean bh,d, however, considerable increase of variance of bh,d in the case of European beech. In contrast to the fumigation period 2000–2007, the non-fumigated preceding period of 1995 through 1999 resulted in 2O 3 b1O ¼ 0:81ð0:26; n ¼ 8Þ and bh;d 3 ¼ 0:77 ð0:18; n ¼ 11Þ for h;d 1O 2O Norway spruce and bh;d 3 ¼ 0:96 ð0:30; n ¼ 7Þ and bh;d 3 ¼ 0:94 ð0:20; n ¼ 6Þ for European beech. A t-test showed no significance differences between the groups which means that no differences between the reference and fumigated stands existed before the experimental ozone exposure. For this reason, the statistical consistency between both samples in the previous period additionally underlines the change in height–diameter allometry under 2O3 in the case of Norway spruce. Apparently, both Norway spruce and European beech shift their resource allocation under ozone fumigation to height growth at the expense of diameter growth. Stems of Norway spruce alter towards top-heavy, slender, and rather unstable stem shapes. Conversely, European beech does not change the height–diameter allometry significantly; however, it shows an increase in variability of allometric form development under ozone fumigation.

3.3. Does the periodic increment of diameter, basal area, height and volume, or the form factor respond to ozone fumigation (Q3)? In the following, we compare the stand of 2O3 fumigated trees with the trees under ambient ozone on the basis of the increment trend method (Section Q3 in ‘‘Material and methods’’). A reported loss of 10% means, that the growth of the respective sample trees lies 10% below the reference trees even after elimination of initial difference in the previous period before fumigation. The comparison between the periodic growth reactions of different tree dimensions (Fig. 6) shows that Norway spruce reduces diameter (12.22%, 21.90, n ¼ 5) and basal area growth at breast height (17.26%, 14.27, n ¼ 5). The increase of height growth (þ69.28%, 27.81, n ¼ 5) induces together with a decrease in form factor (7.00%, 20.95, n ¼ 5), that mean volume growth (þ2.72%, 31.04, n ¼ 5) does not reflect the growth losses revealed on the basis of diameter increment. Aside from the deviations in height growth (p < 0.05), the change in stem dimension differences is not significant from the reference group. In essence, changes in

height growth compensate for the reductions in growth at the stem basis, so that the whole stem production shows no losses. European beech reacts similarly in diameter (12.20%, 11.80, n ¼ 5) and basal area growth at breast height (12.00%, 12.01, n ¼ 5). However, the increase in height (þ33.20%, 35.35, n ¼ 5) is lower than that for spruce. The form factor (33.40%, 23.55, n ¼ 5) and volume increment (43.55%, 5.26, n ¼ 5) are reduced. The reduction in volume growth is significant (p < 0.05) based on a t-test. Both species show a different reaction pattern. In particular, the dimension height, form, as well as the whole-stem react speciesspecific, whereas the diameter and basal area show analogous reaction. 4. Discussion The forest ecosystems in the pre-alpine lowlands of southern Bavaria used to be dominated by European beech; however, forestry favors Norway spruce which normally would only play a minor role without human interference (Pretzsch and Schu¨tze, 2009). Ozone stress seems to reduce stability of Norway spruce, indicated by the shift of height–diameter allometry towards more slender and top-heavy stem shapes. For the dominating pure stands of Norway spruce in this area, ozone represents an additional stress factor beyond the disturbance by bark beetle, drought, storm and ice-breakage. In contrast, for European beech, which is the natural climax species at sub-mountainous altitudes (Ellenberg, 1996), ozone is a new stress factor the species has to cope with. The 2O3 regime employed at Kranzberg Forest was high relative to current O3 regimes (i.e., 1O3) prevailing in rural areas of central Europe, as latter regimes may be enhanced already by about factor three relative to pre-industrial conditions (Stockwell et al., 1997). This was the case at Kranzberg Forest, where the mean O3 level of 1O3 during the growing seasons of the eight experimental years was 33 nl l1. Nevertheless, 1O3 during years of severe summer drought (like in 2003), when expressed as the cumulative O3 exposure index SUM0 (cf. Matyssek et al., 2007), advanced towards 2O3 levels as occurring during humid years at the study site (Lo¨w et al., 2006). 2O3 was relevant in terms of accomplishing an enhanced chronic O3 exposure regime while preventing unrealistically high, acute O3 episodes. Such a rationale is consistent with prognoses of globally increasing O3 background rather than peak concentrations (Vingarzan, 2004). Still, the actual O3 uptake (i.e., O3 dose) was reduced under 1O3

H. Pretzsch et al. / Environmental Pollution 158 (2010) 1061–1070

a

1067

b

Fig. 6. Reaction of diameter loss pid, basal area loss piba, height loss pih, volume increment loss piv and form factor loss pif under double ambient ozone for (a) Norway spruce and (b) European beech. The wiskers show the standard error.

during drought (and only slightly enhanced under 2O3) relative to that of humid years in each O3 regime upon drought-induced stomatal closure (Lo¨w et al., 2006). Across the experimental years, differences between the two O3 regimes in O3 uptake tended to be proportionally smaller than in O3 exposure as a result of stomatal regulation. 2O3 was in the range of O3 scenarios expected to occur during upcoming decades in eastern Asia during summer months. Given such scenarios, substantial loss in the carbon storage capacity of forest systems is prognosticated as based on modeling approaches (Sitch et al., 2007). 4.1. Detection of diameter growth losses at the individual tree level by the increment trend method (Q1) The increment trend method takes advantage of the fact that, in most damaged stands, some vigorous individuals can still be found from which the normal, i.e., reference growth behavior can be derived. The method implies that variations in the increment levels during the undisturbed reference period are similar to the variation during the period of disturbance. Therefore, the choice of the reference period has some influence on the final result if the offset between means varies. In general, the method is well suited to detect the onset of a disturbance, its effect over time, and the degree of increment loss (Deutscher Verband Forstlicher Forschungsanstalten, 1988). The age-dependent decline of radial increment in both tree species, irrespective of the O3 regime (Figs. 3 and 4), was exacerbated in 2003, the year of exceptional summer drought in central Europe (Ciais et al., 2005). This was the case, in particular, in spruce which displayed, in addition, inhibited radial growth during subsequent humid years, indicating after-effects of the drought year (Fig. 3). The higher above-ground sensitivity of spruce to drought was consistent with inhibitions of fine-root productivity and autotrophic soil respiration underneath trees (Nikolova et al., 2009), questioning the growth potential of spruce relative to beech in view of predicted seasonal water limitation during upcoming decades (Beierkuhnlein and Foken, 2008; Geßler et al., 2007). 4.2. Tree height–diameter allometry bh,d under ozone fumigation (Q2) Studies about ozone effects on tree growth focus either on tree diameter increment (Karlsson et al., 1997, 2006) or height increment (Braun et al., 2007); growth analysis of total biomass is restricted to seedlings or saplings (Landolt et al., 2000; Matyssek

et al., 1992, 1993) so that conclusions are hardly transferable to mature trees (Kolb and Matyssek, 2001; Matyssek and Innes, 1999; Samuelson and Kelly, 2001). In the 25–30 m high stand of Kranzberg Forest, we had the rare opportunity to measure height as well as diameter increment of spruce and beech trees under ambient and double ambient O3 regimes from 2000 through 2007 by the use of a crane and scaffolding (Ha¨berle et al., 2003). As the study considered stem diameter as well as height increment, our results enable us to investigate whether or not mature trees under ozone stress alter their matter allocation into height vs. diameter. By application of the allometric exponent bh,d rather than absolute growth rates of height and diameter, we eliminated size effects from the analysis (Pretzsch, 2006). Under 2O3 Norway spruce changes allometry significantly towards slender stem shapes. This outcome was not due to an increase of height increment but a considerable reduction of radial stem growth. Compared to the formation of new buds, leaves, shoots, and fine roots, carbon allocation in stem wood has relatively low priority. Due to the low allocation priority of the stem, diameter increment at breast height is a particularly sensitive, even though unspecific indicator of tree resource availability. Supposing equal tree size, a high diameter increment indicates a reasonable balance in carbon allocation, whereas a low increment indicates a shortage of building material (Waring and Schlesinger, 1985). Clearly, increment at stem base is appropriate for early detection of stress and vitality decline (Dobbertin, 2005; Schweingruber et al., 1983). Kramer (1986) and Sterba (1996) show growth declines particularly in the lower third of the stem during stress for Norway spruce, Scots pine, and silver fir. Elling (1993) and Schweingruber et al. (1983) detected up to 20 missing tree rings at diameter at breast height by means of year ring analysis. However, a decline in increment at stem base is not representative for the whole stem, least of all for the whole tree. Under stress, tree rings in the lower part of the stem can be missing or rather narrow (Elling, 1993; Pollanschu¨tz, 1975, 1980; Rubner, 1910), while tree rings in the upper stem sections are still complete and normal. Therefore, conclusions extrapolating a particular decline in increment at breast height to the whole stem, or even to the whole tree, could result in an overestimation of the growth decline. 4.3. Do the mean periodic annual increment of diameter, basal area, height and volume, or the form factor show a reaction after ozone fumigation (Q3)? Reduction of stem growth as a consequence of ozone exposition is not a novel finding (Matyssek et al., 1992, 1993). For example,

1068

H. Pretzsch et al. / Environmental Pollution 158 (2010) 1061–1070

McLaughlin and Dowing (1995) found 7–30% circumference growth reduction, Karnosky et al. (2005) detected 10–15% decrease in both height and diameter growth and Chappelka and Samuelson (1998) up to 10% reduction of above-ground volume growth. These findings, however, are of limited value, when not presented in concert with studies on height growth and volume increment, allowing for a clearer view on the actual loss in biomass allocation. However, studies showing height growth in relation to ozone are rare (Karnosky et al., 2005). The presented data allow for estimation of the development of the stem volume, which represents the biggest part of the biomass of a mature tree. In our study, Norway spruce showed a (not statistically significant) loss of stem diameter and basal area increment at breast height of about 12% under ozone exposure, which matches the findings of Karlsson et al. (2006) and Wipfler et al. (2005). The height growth of spruce is significantly promoted (70%), resulting in a slight decrease of the form factor. That means stems are developing towards a slender, cone-shaped form (Fig. 7). This result supports the assumption, that wood formation on the lower part of the stem has a low priority when stress occurs. This finding is corresponding to the results of Bartholomay et al. (1997) who found a similar reaction of white pine under ozone exposure. The value of the greatest economical interest is the absolute stem volume increment, which is not reduced by ozone because the decrease in basal area growth is compensated by the increased height growth and change in form factor. European beech exhibits a similar reduction of radial stem increment and increment of basal area (12% and 17%, respectively). This finding is contrary to other studies, performed on the same site, but with different measurement methods and based on a shorter survey period, where no stem growth reduction was observed (Matyssek et al., 2007). The increment of height in beech is not as pronounced as in the case of spruce and the form factor decreases, leading to rather neiloidal stem shapes (Fig. 7) and resulting in clearer loss of stem volume increment, on average of 44%. The results show the importance of allometric studies as a base for scaling up from individual tree to stand level. Altered allometry was already found when root/shoot ratios under ozone influence were scrutinized (Grantz et al., 2006; Landolt et al., 2000; Matyssek and Sandermann, 2003), exhibiting the potential of woody plants to alter the allometry of the whole plant.

5. Conclusions From our results we draw conclusions concerning the methods for detection of growth reactions and the relevance of the revealed disturbances of Norway spruce and European beech forests for ecology and forest management. Ozone-fumigated Norway spruce can change biomass allocation pattern and allometry in a way that stems get more cone-shaped. They reduce biomass investment in the lower stem part first, so that the allocation key changes in favor of upper stem sections and crown growth. European beech changes stem shape the other way around; its form factor decreases under ozone stress and the stem shape becomes more neiloidal. In other words, assessment of growth reactions or even growth losses on whole-tree level should be based not only on diameter or basal area measurement but also take into consideration changes of height growth and stem shape. In our study Norway spruce shows a distinct diameter growth reduction at the reference height of 1.30 m; however considering the increase in height growth, the volume growth even increased slightly. So, while measurement of single measures like height growth, diameter growth or basal area growth have considerable value as indicators, the naive application for upscaling to economical relevant volume growth can be flawed as long as behavior of height and stem form are neglected. In the region studied, forest management started to transfer formerly Norway spruce dominated stands to mixed stands of European beech and Norway spruce. This ozone fumigation experiment represents such a mixture of European beech and Norway spruce. As both species show different reactions to ozone, interspecies competition may change in mixed stands. So the direct growth reduction effect of ozone may be followed by an indirect effect caused by a downward trend of competitive power and access to resources of one or both species in the more popular mixture of European beech and Norway spruce. Even presently instable, further reduction of competition and growth will make the stand dynamics of such stands more unpredictable and call a successful cultivation of pure and mixed stands of both species into question. On tree level ozone fumigation caused increased volume growth of 2.7% in the case of Norway spruce and a decrease of 43.5% in European beech. Applied to the portion of the experimental stand unaffected by ozone, the results would lead to a mean annual volume increase of about 0.7 m3 ha1 yr1 for Norway spruce and a loss of about 10.2 m3 ha1 yr1 for European beech, respectively (Table 1). We speculate that the slight plus in the case of Norway spruce results from competitive reduction caused by the significant productivity loss of neighboring beech. Competitiveness of beech, in mixed stands often obstructive for spruce, seems to be reduced by ozone fumigation. The productivity increase for Norway spruce compensates only to a minor extent for the productivity loss in European beech. Given the economical importance of these species for mid-European forestry, the effect of ozone may lead to severe losses in economical terms and in regional carbon sink strength (Sitch et al., 2007). Acknowledgements

Fig. 7. Change of allometry of Norway spruce and European beech under ozone stress.

The authors wish to thank the Deutsche Forschungsgemeinschaft for providing funds for forest growth and yield research as part of the Sonderforschungsbereich SFB 607 ‘‘Growth and Parasite Defense’’ and the Bavarian State Ministry for Agriculture and Forestry for permanent support of the project W 07 ‘‘Long-term experimental plots for forest growth and yield research’’. Thanks are also due to Gerhard Schu¨tze for support of the field work and the data processing, Ulrich Kern for the graphical artwork, and two anonymous reviewers for their constructive criticism.

H. Pretzsch et al. / Environmental Pollution 158 (2010) 1061–1070

References Ashmore, M.R., 2005. Assessing the future global impacts of ozone on vegetation. Plant, Cell and Environment 28, 1–16. Bartholomay, G.A., Eckert, R.T., Smith, K.T., 1997. Reductions in tree-ring widths of white pine following ozone exposure at Acadia National Park, Maine, U.S.A. Canadian Journal of Forest Research 27, 361–368. Beierkuhnlein, C., Foken, T. (Eds.), 2008. Klimawandel in Bayern. Auswirkungen und ¨ kologie Band, vol. 113. BayCEER, Anpassungsmo¨glichkeiten. Bayreuther Forum O Universita¨t Bayreuth. Braun, S., Schindler, Ch., Rihm, B., Flu¨ckiger, W., 2007. Shoots growth of mature Fagus sylvatica and Picea abies in relation to ozone. Environmental Pollution 146, 624–628. Broadmeadow, M., Heath, J., Randle, T.J., 1999. Environmental limitations to O3 uptake – some key results from young trees growing at elevated CO2 concentrations. Water, Air, Soil, and Pollution 116, 299–310. Chappelka, A.H., Samuelson, L.J., 1998. Ambient ozone effects on forest trees of the eastern United States: a review. New Phytologist 139, 91–108. Ciais, Ph., Reichstein, M., Viovy, N., Granier, A., Oge´e, J., Allard, V., Aubinet, M., Buchmann, N., Bernhofer, Chr., Carrara, A., Chevallier, F., De Noblet, N., Friend, A.D., Friedlingstein, P., Gru¨nwald, T., Heinesch, B., Keronen, P., Knohl, A., Krinner, G., Loustau, D., Manca, G., Matteucci, G., Miglietta, F., Ourcival, J.M., Papale, D., Pilegaard, K., Rambal, S., Seufert, G., Soussana, J.F., Sanz, M.J., Schulze, E.D., Vesala, T., Valentini, R., 2005. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–534. Clark, A.J., Landolt, W., Bucher, J.B., Strasser, R.J., 2000. Beech (Fagus sylvatica) response to ozone exposure assessed with a chlorophyll a fluorescence performance index. Environmental Pollution 109, 501–507. Deckmyn, G., Op de Beeck, M., Lo¨w, M., Then, C., Verbeeck, H., Wipfler, P., Ceulemans, R., 2007. Modelling ozone effects on adult beech trees through simulation of defence, damage and repair costs: implementation of the CASIROZ ozone model in the ANAFORE forest model. Plant Biology 9, 320–330. Deutscher Verband Forstlicher Forschungsanstalten, 1988. Empfehlungen zur ertragskundlichen Aufnahme- und Auswertungsmethodik fu¨r den Themenkomplex ‘‘Waldscha¨den und Zuwachs’’. Allgemeine Forst- und Jagdzeitung 159, 115–116. Dixon, M., Thiec, D.L., Garrec, J.P., 1998. Reaction of Norway spruce and beech trees to 2 years of ozone exposure and episodic drought. Environmental and Experimental Botany 40, 77–91. Dizengremel, P., 2001. Effects of ozone on the carbon metabolism of forest trees. Plant Physiology and Biochemistry 39, 729–742. Dobbertin, M., 2005. Tree growth as indicator of tree vitality and of tree reaction to environmental stress: a review. European Journal of Forest Research 124, 319–333. Ellenberg, H., 1996. Vegetation Mitteleuropas mit den Alpen, fifth ed. Ulmer Verlag, Stuttgart. Elling, W., 1993. Immissionen im Ursachenkomplex von Tannenscha¨digung und Tannensterben. Allgemeine Forstzeitschrift 48, 87–95. Geßler, A., Keitel, C., Kreuzwieser, J., Matyssek, R., Seiler, W., Rennenberg, H., 2007. Potential risks for European beech (Fagus sylvatica L.) in a changing climate. Trees 21, 1–11. Grantz, D.A., Gunn, S., Vu, H.-B., 2006. O3 impacts on plant development: a metaanalysis of root/shoot allocation and growth. Plant, Cell and Environment 29, 1193–1209. Ha¨berle, K.-H., Reiter, I.M., Nunn, A.J., Gruppe, A., Simon, U., Gossner, M., Werner, H., Leuchner, M., Heerdt, C., Fabian, P., Matyssek, R., 2003. KROCO, Freising, Germany: canopy research in a temperate mixed forest of southern Germany. In: Basset, Y., Horlyck, V., Wright, S.J. (Eds.), Studying Forest Canopies from Above: the International Canopy Crane Network. Smithsonian Tropical Research Institute and UNEP, pp. 71–78. Jonson, J.E., Simpson, D., Fagerli, H., Solberg, S., 2006. Can we explain the trends in European ozone levels? Atmospheric Chemistry and Physics 6, 51–66. Karlsson, P.E., Medin, E.L., Wallin, G., Sellde´n, G., Ska¨rby, L., 1997. Effects of ozone and drought stress on the physiology and growth of two clones of Norway spruce (Picea abies). New Phytologist 136, 265–275. ¨ rlander, G., Langvall, O., Uddling, J., Hjorth, U., Wiklander, K., Karlsson, P.E., O Areskoug, B., Grennfelt, P., 2006. Negative impact of ozone on the stem basal area increment of mature Norway spruce in south Sweden. Forest Ecology and Management 232, 146–151. Karnosky, D.F., Pregitzer, K.S., Zak, D.R., Kubiske, M.E., Hendrey, G.R., Weinstein, D., Nosal, M., Percy, K.E., 2005. Scaling ozone responses of forest trees to the ecosystem level in a changing climate. Plant, Cell and Environment 28, 965–981. Karnosky, D.F., Werner, H., Holopainen, T., Percy, K., Oksanen, T., Oksanen, E., Heerdt, C., Fabian, P., Nagy, J., Heilman, W., Cox, R., Nelson, N., Matyssek, R., 2007. Free-air exposure systems to scale up ozone research to mature trees. Plant Biology 9, 181–190. King, J.S., Kubiske, M.E., Pregitzer, K.S., Hendrey, G.R., McDonald, E.P., Giardina, C.P., Quinn, V.S., Karnosky, D.F., 2005. Tropospheric O3 compromises net primary production in young stands of trembling aspen, paper birch and sugar maple in response to elevated atmospheric CO2. New Phytologist 168, 623–636. Kolb, T.E., Matyssek, R., 2001. Limitations and perspectives about scaling ozone impact in trees. Environmental Pollution 115, 373–393. Kramer, H., 1986. Beziehungen zwischen Kronenschadbild und Volumenzuwachs bei erkrankten Fichten. Allgemeine Forst- und Jagdzeitung 157, 22–27.

1069

Landolt, W., Bu¨hlmann, U., Bleuler, P., Bucher, J.B., 2000. Ozone exposure-response relationships for biomass and root/shoot ratio of beech (Fagus sylvatica), ash (Fraxinus excelsior), Norway spruce (Picea abies) and Scots pine (Pinus sylvestris). Environmental Pollution 109, 473–478. Laurence, J.A., Retzlaff, W.A., Kern, J.S., Lee, E.H., Hogsett, W.E., Weinstein, D.A., 2001. Predicting the regional impact of ozone and precipitation on the growth of loblolly pine and yellow poplar using linked TREGRO and ZELIG models. Forest Ecology and Management 146, 247–263. Liu, X., Kozovits, A.R., Grams, T.E.E., Blaschke, H., Rennenberg, H., Matyssek, R., 2004. Competition modifies effects of enhanced ozone/carbon dioxide concentrations on carbohydrate and biomass accumulation in juvenile Norway spruce and European beech. Tree Physiology 24, 1045–1055. Lo¨w, M., Herbinger, K., Nunn, A.J., Ha¨berle, K.-H., Leuchner, M., Heerdt, C., Werner, H., Wipfler, P., Pretzsch, H., Tausz, M., Matyssek, R., 2006. Extraordinary drought of 2003 overrules ozone impact on adult beech trees (Fagus sylvatica). Trees 20, 539–548. Maurer, S., Matyssek, R., 1997. Nutrition and the ozone sensitivity of birch (Betula pendula), II. Carbon balance, water-use efficiency and nutritional status of the whole plant. Trees 12, 11–20. Matyssek, R., Innes, J.L., 1999. Ozone – a risk factor for trees and forests in Europe? Water, Air, Soil, and Pollution 116, 199–226. Matyssek, R., Sandermann, H., 2003. Impact of ozone on trees: an ecophysiological perspective. Progress in Botany 64, 349–404. Matyssek, R., Gu¨nthardt-Goerg, M.S., Saurer, M., Keller, T., 1992. Seasonal growth, d13C in leaves and stem, and phloem structure of birch (Betula pendula) under low ozone concentrations. Trees 6, 69–76. Matyssek, R., Gu¨nthardt-Goerg, M.S., Landolt, W., Keller, T., 1993. Whole-plant growth and leaf formation in ozonated hybrid poplar (Populus x euramericana). Environmental Pollution 81, 207–212. Matyssek, R., Agerer, R., Ernst, D., Munch, J.-C., Osswald, W., Pretzsch, H., Priesack, E., Schnyder, H., Treutter, D., 2005. The plant’s capacity in regulating resource demand. Plant Biology 7, 560–580. Matyssek, R., Bahnweg, G., Ceulemans, R., Fabian, P., Grill, D., Hanke, D.E., Kraigher, H., Osswald, W., Rennenberg, H., Sandermann, H., Tausz, M., Wieser, G., 2007. Synopsis of the CASIROZ case study: carbon sink strength of Fagus sylvatica L. in a changing environment – experimental risk assessment of mitigation by chronic ozone impact. Plant Biology 9, 163–180. McLaughlin, S.B., Dowing, D.J., 1995. Interactive effects of ambient ozone and climate measured on growth of mature forest trees. Nature 374, 252–254. Meehl, G.A., Stocker, T.F., Collins, W.D., Friedlingstein, P., Gaye, A.T., Gregory, J.M., Kitoh, A., Knutti, R., Murphy, J.M., Noda, A., Raper, S.C.B., Watterson, I.G., Weaver, A.J., Zhao, Z.-C., 2007. Global climate projections. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L. (Eds.), Climate Change 2007: the Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. Morgan, P.B., Mies, T., Bollero, G., Nelson, R.L., Long, S.P., 2006. Season-long elevation of ozone concentration to projected 2050 levels under fully open-air conditions substantially decreases the growth and production of soybean. New Phytologist 170, 333–343. Nikolova, P.S., Raspe, S., Andersen, C.P., Mainiero, R., Blaschke, H., Matyssek, R., Ha¨berle, K.-H., 2009. Effects of the extreme drought in 2003 on soil respiration in a mixed forest. European Journal of Forest Research 128, 87–98. Nunn, A.J., Reiter, I.M., Ha¨berle, K.-H., Werner, H., Langenbartels, C., Sandermann, H., Heerdt, C., Fabian, P., Matyssek, R., 2002. ‘‘Free-air’’ ozone canopy fumigation in an old-growth mixed forest: concept and observations in beech. Phyton 42, 105–119. Nunn, A.J., Reiter, I.M., Ha¨berle, K.-H., Langebartels, C., Bahnweg, G., Pretzsch, H., Sandermann, H., Matyssek, R., 2005a. Response patterns in adult forest trees to chronic ozone stress: identification of variations and consistencies. Environmental Pollution 136, 365–369. Nunn, A.J., Kozovits, A.R., Reiter, I.M., Heerdt, C., Leuchner, M., Lu¨tz, C., Liu, X., Lo¨w, M., Winkler, J.B., Grams, T.E.E., Ha¨berle, K.-H., Werner, H., Fabian, P., Rennenberg, H., Matyssek, R., 2005b. Comparison of ozone uptake and sensitivity between a phytotron study with young beech and a field experiment with adult beech (Fagus sylvatica). Environmental Pollution 137, 494–506. Penkett, S.A., 1988. Increased tropospheric ozone. Nature 332, 204–205. Pollanschu¨tz, J., 1975. Zuwachsuntersuchungen als Hilfsmittel der Diagnose und Beweissicherung bei Forstscha¨den durch Luftverunreinigungen. Allgemeine Forstzeitung 86, 187–192. Pollanschu¨tz, J., 1980. Jahrringmessung und Referenzpru¨fung: Ein Beitrag zur Frage der Zuverla¨ssigkeit bestimmter Verfahren der Zuwachsermittlung. Mitteilungen der Forstlichen Bundesversuchsanstalt Wien 130, 263–285. Pretzsch, H., 2006. Species-specific allometric scaling under self-thinning. Evidence from long-tern plots in forest stands. Oecologia 146, 572–583. Pretzsch, H., 2009. Forest Dynamics, Growth and Yield. Springer, Berlin, Heidelberg, pp. 560–565. Pretzsch, H., Schu¨tze, G., 2005. Crown allometry and growing space efficiency of Norway spruce (Picea abies (L.) Karst.) and European beech (Fagus sylvatica L.) in pure and mixed stands. Plant Biology 7, 628–639. Pretzsch, H., Schu¨tze, G., 2009. Transgressive overyielding in mixed compared with pure stands of Norway spruce and European beech in central Europe: evidence on stand level and explanation on individual tree level. European Journal of Forest Research 128, 183–204.

1070

H. Pretzsch et al. / Environmental Pollution 158 (2010) 1061–1070

Pretzsch, H., Kahn, M., Grote, R., 1998. Die Fichten-Buchen-Mischbesta¨nde des Sonderforschungsbereiches ‘‘Wachstum oder Parasitenabwehr?’’ im Kranzberger Forst. Forstwisschaftliches Centralblatt 117, 241–257. Prodan, M., 1951. Messung der Waldbesta¨nde. JD Sauerla¨nder’s Verlag, Frankfurt am Main, pp. 18, 186–203. Rubner, K., 1910. Das Hungern des Cambiums und das Aussetzen der Jahrringe. Naturwissenschaftliche Zeitschrift Forst- und Landwirtschaft 8, 212–262. Samuelson, L., Kelly, J.M., 2001. Scaling ozone effects from seedlings to forest trees. Tansley Review No. 21. New Phytologist 149, 21–41. Sandermann, H., Ernst, D., Heller, W., Langebartels, C., 1998. Ozone: an abiotic elicitor of plant defence reactions. Trends in Plant Science 3, 47–50. Schweingruber, F.H., Kontic, R., Winkler-Seifert, A., 1983. Eine jahrringanalytische Studie zum Nadelbaumsterben in der Schweiz. Berichte der Eidgeno¨ssichen Anstalt fu¨r das forstliches Versuchswesen 253, 29. Sitch, S., Cox, P.M., Collins, W.J., Huntingford, C., 2007. Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature 448, 791–794. Ska¨rby, L., Ro-Poulsen, H., Wellburn, F.A.M., Sheppard, L.J., 1998. Impacts of ozone on forests: a European perspective. New Phytologist 139, 109–122. Somers, G.L., Chappelka, A.H., Rosseau, P., Renfo, J.R., 1998. Empirical evidence of growth decline related to visible ozone injury. Forest Ecology and Management 104, 129–137. Sterba, H., 1996. Forest decline and growth trends in central Europe. In: Spiecker, H., Mielika¨inen, K., Ko¨hl, M., Skovsgaard, J.P. (Eds.), Growth Trends in European Forests. Springer, Berlin, Heidelberg, New York, pp. 149–165.

Stockwell, W.R., Kramm, G., Scheel, H.-E., Mohnen, V.A., Seiler, W., 1997. Ozone formation, destruction and exposure in Europe and the United States. In: Sandermann Jr., H., Wellburn, A.R., Heath, R.L. (Eds.), Forest Decline and Ozone: a Comparison of Controlled Chamber and Field Experiments. Ecological Studies, vol. 127. Springer, Berlin, Heidelberg, New York, pp. 1–38. Taylor, G.E., Johnson, D.W., Andersen, C.P., 1994. Air pollution and forest ecosystems: a regional to global perspective. Ecological Applications 4, 662–689. Vingarzan, R., 2004. A review of surface ozone background levels and trends. Atmospheric Environment 38, 3431–3442. Vollenweider, P., Woodcock, H., Keltry, M.J., Hofer, R.-M., 2003. Reduction of stem growth and site dependency of leaf injury in Massachusetts black cherries exhibiting ozone symptoms. Environmental Pollution 125, 467–480. Volz, A., Kley, D., 1988. Evaluation of the Montsouris series of ozone measurements made in the nineteenth century. Nature 332, 240–242. Von Bertalanffy, L., 1951. Theoretische Biologie: II. Band, Stoffwechsel, Wachstum, second ed. A Francke AG, Bern, pp. 311–315. Waring, R.H., Schlesinger, W.H., 1985. Forest Ecosystems: Concepts and Management. Academic Press, Orlando. Werner, H., Fabian, P., 2002. Free-air fumigation of mature trees – a novel system for controlled ozone enrichment in grown-up beech and spruce canopies. Environmental Science and Pollution Research 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 Biology 7, 611–618.