Contribution of ambient ozone to Scots pine defoliation and reduced growth in the Central European forests: A Lithuanian case study

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Environmental Pollution 155 (2008) 436e445 www.elsevier.com/locate/envpol

Contribution of ambient ozone to Scots pine defoliation and reduced growth in the Central European forests: A Lithuanian case study Algirdas Augustaitis a,*, Andrzej Bytnerowicz b a

Lithuanian University of Agriculture, Forest Monitoring Laboratory, Studentu 13, LT-53362 Kaunas dstr., Lithuania b USDA Forest Service, 4955 Canyon Crest Drive, Riverside, CA 92507, USA Received 29 January 2008; accepted 30 January 2008

Peak ozone concentrations is one of the key factors affecting Scots pine trees. Abstract The study aimed to explore if changes in crown defoliation and stem growth of Scots pines (Pinus sylvestris L.) could be related to changes in ambient ozone (O3) concentration in central Europe. To meet this objective the study was performed in 3 Lithuanian national parks, close to the ICP integrated monitoring stations from which data on meteorology and pollution were provided. Contribution of peak O3 concentrations to the integrated impact of acidifying compounds and meteorological parameters on pine stem growth was found to be more significant than its contribution to the integrated impact of acidifying compounds and meteorological parameters on pine defoliation. Findings of the study provide statistical evidence that peak concentrations of ambient O3 can have a negative impact on pine tree crown defoliation and stem growth reduction under field conditions in central and northeastern Europe where the AOT40 values for forests are commonly below their phytotoxic levels. Ó 2008 Elsevier Ltd. All rights reserved. Keywords: Peak ozone concentration; Acidifying compounds; Meteorological parameters; Scots pine; Basal area increment; Defoliation

1. Introduction Ambient ozone (O3) is considered to be one of the most important and pervasive phytotoxic agents whose effects are likely to increase in the future (Krupa and Manning, 1988; Hutunnen et al., 2002; Percy et al., 2003; Vingarzan, 2004). Its effects on plants are the result of a three-step chain of events: exposure, uptake, and biological effect (Tausz et al., 2006). Ozone can cause a wide range of symptoms: increase in respiration (Reich, 1983), mineral nutrient deficiencies (Schmieden and Wild, 1995; Utrainen and Holopainen, 2000), decrease in foliar chlorophyll content and development of necrotic spots (Reich, 1983; Smith, 1981; Chappelka et al., 1999), acceleration of leaf senescence and reduction in leaf life-span (Pell et al., 1999; Skelly et al., 1999; Stow et al., 1992), reduction in photosynthesis (Reich, 1983; Reich and Amundson, 1985; Utrainen and Holopainen, 2000), and ultimately reduced

* Corresponding author. Tel.: þ370 37 752367; fax: þ370 37 752379. E-mail address: [email protected] (A. Augustaitis). 0269-7491/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2008.01.042

growth and productivity (Karnosky et al., 1996, 2006; Laurence, 1998; Matyssek and Innes, 1999; Manning, 2005). Leaf and needle drop (reduction in foliage biomass, defoliation), and reduction in stem increment (radial or basal area) were chosen as the main objects in order to explore the possible effect of O3 on trees. Forest monitoring usually concentrates on these non-specific response indicators, which are the object of many stressors other than O3. However, due to the expected increase in future ambient O3 concentrations (Fowler et al., 1999; Percy et al., 2003) it is necessary to determine if exposure to ambient O3 levels actually affects tree growth and crown condition in natural forests (Manning, 2005). Acid rain and ambient O3 are among the key factors resulting in spatial and temporal changes of tree crown defoliation (Reich, 1987; Guderian, 1985; Takemoto et al., 2001; Sandermann, 1996). Their combined effects differ significantly from the sum of individual effects due to their complex synergistic or antagonistic interactions (Bytnerowicz et al., 2007). Therefore, the process base of O3 damage to plants is still not fully clarified (Zierl, 2002; Matyssek et al., 2005) and the relationship between forest tree crown condition and O3 effects is still not well established

A. Augustaitis, A. Bytnerowicz / Environmental Pollution 155 (2008) 436e445

(Manning, 2005; Ollinger et al., 1997; Percy and Ferretti, 2004; Paoletti, 2006). Most of the authors investigating O3 effects on forests suggest a need for studying O3 impacts in the context of other environmental factors (Kolb and Matyssek, 2001). Relationships between ambient O3 and tree growth, focusing on physiological or biochemical effects on tree seedlings, have been extensively documented in artificial conditions (Chappelka and Samuelson, 1998; Ska¨rby et al., 1998; Krupa and Kicker, 1989; Manning et al., 2004). However, too little is known about the effect of O3 on tree growth on a regional scale, where its effects may be subtle and difficult to detect (Paoletti, 2006; Percy and Ferretti, 2004) and studies often fail despite using sophisticated statistically-based approaches (Muzika et al., 2004). Data obtained in artificial conditions do not apply well to actual forest conditions and the growth of large trees (Sandermann, 1996; Manning, 2005; Kolb and Matyssek, 2003). Due to differences in the physiological behavior of seedlings vs. adult trees and chamber effects, extrapolation of these results to trees in the forest is impossible (Kolb et al., 1997; Manning, 2005). Effects of O3 exposure have to be evaluated in the context of changing climate, i.e. increasing temperature, changes in water availability, increasing CO2 concentrations, increased available nitrogen [N] due to elevated levels of N deposition, and many other factors (Bytnerowicz et al., 2007). In this study we attempted to investigate the possible effect of natural and anthropogenic environmental factors on pine defoliation and stem growth, and quantify O3 contributions to the integrated impact of these factors. A working hypothesis was that in the central European forests peak O3 concentration could be one of the key factors resulting in Scots pine defoliation and stem increment reduction, reinforcing the effects of the other natural and anthropogenic stresses. 2. Materials and methods Data on Scots pine (Pinus sylvestris L.) from permanent observation stands (POS) of the local forest monitoring network in National Parks over the period since integrated monitoring (IM) stations have been in operation (Aukstaitija IMS, LT-01; Dzukija IMS, LT-02; Zemaitija IMS, LT-03) were used.

437

2.1. Response variables To get more insight into the relationships between different O3 indices and pine defoliation, annual defoliation data from 48 pine POS located close to the integrated monitoring stations for a 12 year period in Aukstaitija and Zemaitija National Parks (NP) and a 6 year period (1994e1999) in Dzukija NP were used as a response variable. In 2000, due to limited funding, the Dzukija NP station was closed and the monitoring terminated. Pine stands were selected according to stand maturity: 8 sapling stands (45e 50 years), 10 middle aged stands (61e80 years), 11 premature stands (81e 100 years), 11 mature stands (101e120 years) and 8 over mature stands (>121eyears). Data on tree and stand parameters (mean diameter and height of trees, tree density, basal area and tree volume per hectare) as well as crown defoliation were available from the permanent observation stands. A three-stage sampling pattern was used for the collection of the field material: (i) sampling of the research stands; (ii) sampling of the circular plots within each research stand; (iii) sampling of the trees for more detailed measurements of tree crown parameters and tree ring analysis. Each pine stand included 12 circular sample plots with on average 15e20 trees in each plot, i.e., about 150e250 sample trees. The sample plots were distributed systematically in a grid system. Crown defoliation of more than 8000 pine trees was assessed annually at the end of August through the beginning of September. The ICP Forest monitoring methodology was employed to assess tree defoliation (UN-ECE, 1994). From this POS set we chose 12 mature and premature observation stands located closest to IM stations to quantify O3 contribution to the integrated impact of the considered environmental factors on pine stem basal area increment (Table 1). More than 200 dominant and co-dominant trees, for which crown defoliation had been assessed since 1994, were chosen for the increment boring.

2.2. Predictor variables and methods of their estimation The considered predictor variables were classified into 3 groups. The first group included 3 site-specific variables(forest type, soil typological groups with respect to fertility, and moisture conditions) and 5 tree and stand variables (mean tree age, height, diameter, basal area, and stand volume). These data were available from the permanent observation stands and were collected using the same 3-stage sampling pattern. The second group consisted of 10 meteorological variables (air temperature and amount of precipitation for 8 seasons of 2 years and 2 year-long periods from September to August). These data were collected at IM stations according to the requirements of the WMO Guidelines (1989) to ensure their comparability with the data from official weather stations and other monitoring sites. The third group of 13 variables included data on: air concentrations of sulfur dioxide (SO2), sulfate (SO2 4 ), the sum of nitrates in aerosols and gaseous nitric

Table 1 Characteristics of the considered permanent observation stands (POS) POS

Stand and site parameters Mean height (m)

Sum of basal area (m2 ha1)

Volume (m3 ha1)

Tree density (unit ha1)

Forest type

Aukstaitija National Park ANP-1 170 41.4 ANP-2 60 18.5 ANP-3 170 42.4 ANP-4 60 17.8 ANP-5 170 41.7 ANP-6 60 16.6

29.5 19.7 31.0 19.4 29.9 17.1

31.0 17.2 32.0 17.5 27.8 19.6

417 173 456 175 381 177

221 600 220 622 194 772

Vac-myr Vac-myr Vac-myr Vac-myr Vac-myr Vac-myr

Zemaitija National Park ZNP-1 110 392 ZNP-2 110 379 ZNP-3 100 315

289 282 248

26.0 35.9 25.8

301 402 264

134 198 152

Myr-ox Myrtil Myrtil

Dzukija DNP-1 DNP-2 DNP-3

17.4 17.3 20.9

27.2 22.2 31.0

246.4 200.8 307.8

1156 413 442

Clad Clad Vac

Age (years)

National Park 50 70 70

Mean diameter (cm)

17.3 26.1 29.9

Forest type: Vac-myr, Pinetum vacciniosum-myrtilosum; Myr-ox, P. myrtilosum-oxalidosum; Myrtil, P. myrtilosum; Clad, P. cladoniosum; Vac, P. vacciniosum.

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P  acid ( NO 3 ¼ NO3 þ HNO3) and the sum of gaseous ammonia and ammoP þ 2  nium in aerosols ( NHþ 4 ¼ NH3 þ NH4 ); concentration of SO4 , NO3 , þ NHþ and H in precipitation as well as their wet deposition (Sopauskiene and 4 Jasineviciene, 2006). The air sampling at IM stations was carried out at weekly intervals. The sampling equipment for SO2 and particulate sulfate consisted of a 2-stage filter pack sampler with a Whatman 40 cellulose filter. SO2 was collected by retention of particles P using a Whatman P þ 40 filter impregnated with potassium hydroxide (KOH). NO NH4 were collected using an open3 and face separate sampler with alkaline (KOH) and oxalic acid impregnated Whatman 40 filters, respectively (Sopauskiene and Jasineviciene, 2006). Precipitation samples at IM stations were collected weekly in a polyethylene bulk-collector from December to March and in an automatic wet-only sampler during the remaining months. All samples were stored at 4  C until laboratory analysis. Ion chromatography using Dionex 2010i with conductivity detection was used for the chemical analysis of anions in precipitation and in water extracts from the impregnated Whatman 40 filters. The NHþ 4 concentration in precipitation as well as in the solutions extracted from Whatman 40 filters impregnated with oxalic acid was analyzed spectrophotometrically, using the indophenol blue method. Precipitation pH and electrical conductivity were determined with a pH glass electrode and an electric conductance meter, respectively (Sopauskiene and Jasineviciene, 2006). At IM stations the measurements and analytical procedures were based on a quality assurance/quality control (QA/QC) program as described in the EMEP CCC manual for sampling, chemical analysis, and quality assessment (EMEP, 1977).

2.3. Statistical analysis of data The integrated impact of the natural and anthropogenic factors on mean defoliation and stem basal area increment of pine trees was analyzed by a multiple stress approach, using the linear multiple regression technique of Statistica 6.0 software. The quality of the created models was assessed by determining the coefficient of determination (R2) and the level of statistical significance ( p). Stress factors were excluded from the regression model by a stepwise procedure based on the level of significance of each stress factor. Finally, variables with a high level of significance compiled the models. The impact of ambient O3 on pine crown defoliation and BAI was examined in a 2-step multi-regression procedure (Neirynck and Roskams, 1999). The annual mean defoliation was regressed on site and stand predictor variables using a stepwise regression with a forward selection procedure. Then, the residual defoliation was regressed on air concentrations of acidifying compounds, their concentration in precipitation and deposition, and meteorology using the same stepwise regression procedure. The annual BAI was regressed on stand predictor variables and crown defoliation using a stepwise regression with a forward selection procedure. Then, the BAI residuals were regressed on air concentrations of acidifying compounds, their concentration in precipitation and deposition, and meteorology using the same stepwise regression procedure. Finally, the predictor variable ‘‘peak ozone concentration’’ was included in the created models and its contribution to the integrated impact of different combinations of natural and anthropogenic factors on pine crown defoliation and BAI was quantified. This index was shown to contribute most significantly to changes in different components of forest biota (Augustaitis et al., 2007b) and to best reflect the changes in AOT40 for vegetation and forest. Correlation coefficient between these parameters made 0.62 and 0.55 respectively when p < 0.05. The key point of the study e separation of the direct O3 effect on tree growth from the integrated effect of acidifying compounds on foliage e was accomplished by means of correlative analysis. Reduction in productivity due to disturbances in transpiration, carbohydrate metabolism and movement and mineral nutrient deficiencies (Reich, 1983; Schmieden and Wild, 1995; Ollinger et al., 1997) seemed to be the most relevant, since changes in growth often occur at levels below the ambient air quality standards or may proceed without signs of the usual leaf damage (LaCoss, 2000). Therefore, the possible direct effect of peak O3 concentration on pine stem basal increment was investigated after the influence of crown defoliation had been accounted for. The Fisher test was used for estimating the significance of the differences in changes in mean defoliation of Scots pine trees, data on pollution and meteorology among NP (spatial changes) as well as within NP (temporal changes).

3. Results 3.1. Changes in ambient ozone and acidifying air compounds and their deposition Data from IMS indicated a significant decrease in air concentrations of sulfur compounds and ammonia and their deposition until 2000 (Fig. 1). The air concentration of SO2 at Aukstaitija IMS (LT-01) decreased by 82% (from 2.73 to 0.49 mg S m3), at Zemaitija IMS (LT-03) by 79% (from 2.22 to 0.47 mg S m3), and at Dzukija IMS (LT-02) by 57% (from 3.0 to 1.3 mg S m3). Wet sulfur deposition at LT-01 decreased by 67% (from 685 to 225 mg S m2), at LT-03 by 58% (from 750 to 312 mg S m2), and at LT-02 by 53% (from 740 to 350 mg S m2) (Augustaitis et al., 2005; Sopauskiene and Jasineviciene, 2006). Afterwards, Pstabilization or some increase was observed. The decrease in NHþ 4 air concentrations and wet deposition P was less pronounced while the air concentration of NO 3 was rather stable. However, since 2001 a tendency towards increasing air concentrations of NO 3 has been detected. Among the NPs, there were statistically significant differences in air concentrations of SO2 ( p < 0.037) and the wet P  2 deposition of NO3 ( p < 0.000) and ( p < 0.035), 4 P SO þ while differences in wet deposition of NH4 were barely significant ( p < 0.058). Consequently, the southern and western parts of Lithuania were more polluted, which is most likely related to the proximity of these territories to the major pollutant sources in central Europe (Augustaitis et al., 2005; Sopauskiene and Jasineviciene, 2006; Augustaitis et al., 2007a). Between 1995 and 2000 peak O3 concentration was decreasing, while between 2001 and 2005 it was increasing. The highest peak O3 value of 213 mg m3 was observed only in the year 1995, while higher than 160 mg m3 value was observed at the beginning of the observation period and recently, in the years 2002 and 2005. Peak O3 concentrations most often were observed in spring, i.e., in April and May (Bycenkiene and Girgzdiene, 2006). The computed AOT40 values for the protection of forest at LT-01 and LT-02 ranged from 4000 to 11,000 ppb h while at LT-03 only from 2500 to 6000 ppb h, and exceeded the critical value for the protection of vegetation (3000 ppb h) for almost all of the considered years. The critical level 10,000 ppb h for the protection of forest was observed only at LT-01 in the year 1999. The newly established AOT40 critical level for forests has been established at 5000 ppb h, therefore the potential for O3 damage is higher than the previous AOT40 critical level of 10,000 ppb h would predict. 3.2. Temporal and spatial changes in meteorology Annual amounts of precipitation among national parks differed significantly ( p < 0.05). Mean annual precipitation was 930 mm at Zemaitija NP, 710 mm at Aukstaitija NP, and 650 mm at Dzukija NP. The precipitation amount from October through February accounted for these differences. However, there were no significant temporal differences in annual precipitation during the 1994e2005 period. The average amount of

A. Augustaitis, A. Bytnerowicz / Environmental Pollution 155 (2008) 436e445

ΣNH4+ 800

600 1.5 400 1.0 200

0

400 4 200 2

mg•m-2

120 40 80 20

40

2005

2004

2003

1999

1998

1997

0 1996

0 1995

2005

2004

2003

2002

2001

2000

0 1999

0.0 1998

100

1997

0.2

160 60

1994

200

0.4

200

80

ΣNO3- μg•m-3

LT 01

LT 02

LT 03

Mean

LT 01

LT 02

LT 03

NO3-

LT 01

LT 02

LT 03

Peak

LT 01

LT 02

LT 03

mg•m-2

Peak Concentration, μg•m-3

300

240

O3

500

-

0.6

1996

2005

LT 03

400

1995

2004

LT 03

LT 02

0.8

1994

2003

LT 02

LT 01

Mean concentration, μg•m-3

NO3

2002

LT 01

LT 03

Deposition, mgN•m-2

Concentration, μgN•m-3

ΣNO3

-

2001

ΣNH4+ μg•m-3 NH4+ 100

1.0

2000

1999

1998

1997

1996

1994

LT 03

2002

LT 02

0

0

2001

LT 02

LT 01

6

2005

2004

2002 2003

2001

2000

1999

LT 01

600

2000

SO2 μg•m-3

1998

1996 1997

1995

1994

0.0

8

1995

0.5

NH4+

Deposition, mgN•m-2

2.0

Deposition, mgS•m-2

Concentration, μgS•m-3

2.5

SO42- mg•m-2

800

10

1000

SO42-

SO2

Concentration, μgN•m-3

3.0

439

Fig. 1. Air concentrations and deposition of the considered pollutants.

precipitation during the autumn and winter seasons was stable, while in spring it decreased by 10.4 mm per season ( p < 0.037) and in summer increased by 13.3 mm per season ( p < 0.010). The mean annual temperature tended to increase between 1994 and 2005 ( p > 0.05). At Aukstaitija there was an average increase of 0.013  C per year, at Dzukija 0.061  C, and at Zemaitija 0.069  C per year. The increase was most pronounced in autumn (SeptembereNovember). The mean annual temperature in Zemaitija (þ6.9  C) was significantly higher than in Aukstaitija (þ6.4  C) and Dzukija (þ6.5  C) ( p < 0.05). 3.3. Temporal and spatial changes in mean defoliation of Scots pines

very serious crown damage. In 1996 biological insecticide Foray-48B was applied to suppress the outbreak, and recovery of the damaged Scots pine trees started. The highest level of mean defoliation of pine trees in Aukstaitija and Dzukija NPs was observed in 1995, whereas in Zemaitija NP it was in 1997 (Fig. 2). Afterwards, crown condition showed obvious improvement that lasted until 2000e2001. Between 2002e2005 pine defoliation started to gradually increase in Zemaitija NP, meanwhile in Aukstaitija NP since 2003 defoliation has decreased. The detected temporal changes in mean defoliation of pine trees were quite common throughout most of Europe (UN-ECE, 2005; Lorenz and Mues, 2007). 3.4. Changes in stem radial increment of Scots pine trees

Scots pine trees in Aukstaitija NP showed the best condition as illustrated in Fig. 2. On the poorest sites (Pinetum cladoniosum forest type) in Dzukija NP, outbreaks of the forest pests (Diprion pini L. and Ocneria monacha L.) started in 1992 after a hot and dry vegetation period in 1991 and caused

Analysis of the Scots pine stem radial increment was performed over the 1994e2003 period. Significant temporal changes in increment were established at all sites ( p < 0.05) (Fig. 3) and reflected changes in crown defoliation (Fig. 2).

A. Augustaitis, A. Bytnerowicz / Environmental Pollution 155 (2008) 436e445

440

meteorology were examined after the influences of secondary natural variables such as site and stand parameters had been accounted for. In our study the correlation between pine defoliation and stand density was found to be the strongest (r ¼ 0.38), followed by a weaker negative correlation with stand volume (r ¼ 0.23), and age (r ¼ 0.19, p < 0.05). Significant differences in defoliation were established among stands from different sites. The highest mean defoliation (36.4%  1.0) was recorded on Pinetum cladoniosum forest type (FT), the lowest on Pinetum vacciniosum FT (19.2%  0.2) and Pinetum oxalidosum FT (19.6%  1.4). Although these parameters cannot affect tree condition directly, their predisposing effects are well known. The integrated impact of these parameters accounted for more than 60% variation in defoliation:

40

Mean defoliation, %

35 30 25 20 15

Zemaitija NP

Aukstaitija NP

2005

2004

2003

2002

2001

2000

1999

1998

1997

1996

1995

1994

10

Dzukija NP

Fig. 2. Mean values and standard errors of pine defoliation in Lithuanian NPs.

F ¼ 11:61 þ 1:378  A  0:169  SG þ 0:012  N þ 1:884

Correlation coefficients ranged between r ¼ 0.25 in Zemaitija and r ¼ 0.91 in Dukija NP, and at an average made r ¼ 0.45. Over the considered period radial increment of the pine stems in Aukstaitija NP increased by an average of 0.033 mm per year in middle aged and 0.018 mm per year in matured stands. In contrast, in Zemaitija NP radial increments of the pine stems decreased by an average of 0.024 mm per year. Over the period from 1994 to 1999 pine stem increment increase in Dzukija NP was the most significant, at an average of 0.178 mm per year (Fig. 3).

 FType; R ¼ 0:610; p < 0:05

3.5. Changes in considered response variables in relation to air pollution and acid deposition A large portion of the defoliation data variance is explained by site and stand indices, thus reducing the potential role of pollutants (Klap et al., 2000; Ozolincius and Stakenas, 2001; De Vries et al., 2003; Ferretti et al., 2003; Ozolincius et al., 2005). Therefore, in order to meet the objectives of the present study, the relationships between pine defoliation, pollution and

2

ð1Þ P where F is crown defoliation (%), A is the stand age (years), G is the sum of the tree basal area (m2 ha1), N is the tree number (units ha1) and FType is the forest type (categorical value). The procedure for accounting for the impact of site and stand indices could be evaluated as having been successful since the significance of the relationships between defoliation residuals, and meteorology, remained at the same level. The significance of the relationship between defoliation residuals and acidifying compounds decreased from 1.5 times (air concentration) to 2 times (deposition), whereas the significance of the relationship between defoliation residuals and peak O3 concentrations increased from 0.315 to 0.439 (Fig. 4). Employing the same procedure, the strongest correlation was established between pine stem basal area increment and crown defoliation (r ¼ 0.512), followed closely by the positive correlation with tree diameter (r ¼ 0.382), and a weaker negative correlation with stand age (r ¼ 0.081). The integrated impact 3.0

Aukstaitija NP (LT-01)

Radial increment, mm

1.0 Matured stands 0.8 0.6 0.4 ANP-3

ANP-1

Middle-aged stands 2.0 1.5 1.0 ANP-4

ANP-2

ANP-5

0.2

ANP-6 2003

2004 2004

2002

2003

2001

2000

1999

1998

1997

1996

1995

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1993

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1989

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2002

2001

2000

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1996

1995

1994

1993

1992

1991

1990

1989

0.5

2.5

2.5 DNP-1 DNP-2 DNP-3

2.0 1.5 1.0 0.5

Zemaitija NP (LT-03)

Radial increment, mm

Dzukija NP (LT-02)

2.0 1.5 1.0 0.5 ZNP-2

ZNP-1

ZNP-3

Fig. 3. Radial increment of pine trees at different sites.

2002

2001

2000

1999

1998

1997

1996

1995

1994

1993

1992

1991

2004

2003

2002

2001

2000

1999

1998

1997

1996

1995

1994

1993

1992

1991

1990

1990

0.0

0.0 1989

Radial increment, mm

Aukstaitija NP (LT-01) 2.5

1989

Radial increment, mm

1.2

A. Augustaitis, A. Bytnerowicz / Environmental Pollution 155 (2008) 436e445 0.8

Zq Zqres p<0.05

Correlation coefficient

0.6

441

F F res p<0.05

0.4 0.2 0 -0.2 -0.4 -0.6 A -0.8

D

Stand indices

SO2

Mean Peak AOT40

NH4+

NO3-

Air concentration

Ozone indices

SO42 -

NH4+

NO3-

Deposition

Fig. 4. Relationships between considered response variables and their residuals with main predictor variables in Lithuanian NPs. Response variables: Zq, basal area increment; F, defoliation; res, residuals. Predictor variables: stand indices: A, age; D, diameter; Ozone indices: mean, annual average; AOT40, for forest).

of these parameters was analyzed using a multiregression model. Crown defoliation (F, %), tree age (A, years) and diameter (D, cm) accounted for 80% of the spatial and temporal variability in pine stem basal area increment (Zq, cm2): Zq ¼ 7:330  0:189  F  0:088  A þ 0:50  D; R2 ¼ 0:795; p < 0:05

ð2Þ

Correlation analysis between BAI residuals and the rest of the considered predictor variables revealed the highest significance for peak ozone impact on increment residuals ( p < 0.001) and the least for acid deposition (Fig. 4). This procedure allowed elimination of the impact of the air concentration of the acidifying compounds and their deposition on BAI through the decrease in foliage thus verifying strong interaction of acid compounds with crown defoliation which was detected not only in our earlier studies, but also in the causeeeffect studies on pine defoliation changes in Europe (Lorenz and Mues, 2007). These findings indicate a possible direct effect of ambient O3 on changes in pine stem increment, probably due to disturbances in CO2 assimilation and carbohydrate movement within the trees. In our opinion, the elimination of the defoliation impact on tree increment by empirical regression methods was a good example of an attempt to separate the effects of different pollutants, i.e., acidifying compounds and ambient O3. The key environmental factor resulting in both crown defoliation and BAI changes after the effect of site and stand indices had been accounted for was found to be peak O3 concentration. The effect of AOT40 index on the considered response variables was distinctly lower. 3.6. Contribution of peak ozone concentrations to pine defoliation and growth reduction Despite the statement that below the phytotoxic level no direct threat to vegetation from SO2 (Hjellbrekke, 1999) or synergetic interaction between SO2 and O3 could be expected (Krupa and Arndt, 1990), the present data confirm our earlier findings that acidifying air compounds and their deposition are the key factors resulting in pine defoliation changes (Augustaitis et al., 2003, 2005, 2007a). They explain from 23% to 28% of the

variance of residual defoliation of pine trees. The effect of peak O3 concentrations was less significant (19.3%), however, they increase the explanation rate of defoliation residual variability by air concentration of acidifying compounds, their concentration in precipitation and deposition from 3 to 8% (Table 2). There was no statistical evidence on the synergetic effect of O3 and SO2 on pine defoliation; peak O3 values reinforced the effect of SO2 on residuals by only 2.4%. However, peak O3 concentrations reinforced the impact of acid deposition and drought on pine defoliation more significantly e by approximately 6% e and the mean temperature of the dormant period by 11%. In any case, when impacts of all considered predictor variables were accounted for, the effect of peak O3 values remained significant ( p < 0.05) increasing the degree of explanation of defoliation residuals variability up to 30%. Generalizing the results presented here the conclusion can be drawn that peak O3 concentrations could be considered as one of the key factors affecting pine crown condition in Lithuania. The integrated impact of air acidifying compounds and their deposition accounted for 18.5% of variability in stem increment residuals. O3 increased the degree of the explanation by 8.7% up to 27.2% (Table 3). Integrated impacts of meteorological parameters accounted for 10.2% of variability of stem increment residuals, and O3 increased this rate up to 17.2% (by 7.0%). Integrated impacts of air acidifying compounds, acid deposition and meteorological parameters accounted for up to 21% of variability in residuals of stem basal area increment. Ozone increased this rate of explanation by approximately 10% up to 31.6%. Thus, we can conclude that the key factor contributing to increment residual changes could have been peak O3 concentrations while SO2 reinforced the O3 effect on stem increment. These results verify the hypothesis that in the regions affected by air pollution, peak O3 values are most likely to be among the key factors affecting spatial and temporal variability of Scots pine defoliation and growth reduction. 4. Discussion The detection of the negative ambient O3 effect on mature trees under field conditions is more complicated than under

A. Augustaitis, A. Bytnerowicz / Environmental Pollution 155 (2008) 436e445

442

Table 2 Contribution of ambient ozone to the integrated impact of different environmental factors on residuals of pine crown defoliation Variables

Models, F(a,b) (1,419)

In the air SO2 P þ PNH4 NO3

(2,418)

(3,417)

(4,416)

(2,418)

(2,418)

(5,415)

þ

(6,414) þ

þ þ

In precipitation SO2 4 NHþ 4 NO 3

þ þ

Deposition SO2 4 NHþ 4 NO 3 Precipitation Last season IXeXI XIIeII IIIeV VIeVIII Current season IXeXI XIIeII IIIeV VIeVIII Temperature Last season IXeXI XIIeII IIIeV VIeVIII Current season IXeXI XIIeII IIIeV VIeVIII r2 (%) r2* with O3 effect (%) O3 effect (r2*  r2) (%) O3 significance, p<

(2,418)

þ

þ þ þ

þ

þ

þ

þ

þ

þ

þ

þ

þ

þ þ

þ

þ þ

25.4 27.7 2.4 0.000

18.1 26.1 8.0 0.000

17.3 23.2 5.9 0.000

20.0 25.7 5.7 0.000

11.5 22.9 11.4 0.000

þ

þ

7.1 19.5 12.4 0.010

18.0 25.8 7.8 0.010

24.0 26.7 2.7 0.000

29.0 29.9 1.0 0.034

Individual impact of peak O3 concentration on defoliation residual: r2 ¼ 19.3% and p < 0.0001. F(a,b), models identified by the F-test symbol with degrees of freedom: a, of the predictor variables; b, of the observations (Statistica software); significance of variables (þ) when p < 0.05.

artificial conditions, where experiments have not yet precisely determined if ambient O3 levels actually impair it (Manning, 2005). Years may be required before ecological change within ecosystems resulting from continuous exposure to toxic airborne concentrations become evident (Szaro et al., 2002). Numerous studies underscore the negative effect of ambient O3 on tree photosynthesis and biomass production under long-term exposure to moderately elevated O3 concentrations (Fuhrer et al., 1997; Ska¨rby et al., 1995). However, only recently the data on the phytotoxic effect of regional O3 concentration on forests in central and northern Europe have been presented more often (Karlsson et al., 2006; Bytnerowicz et al., 2004; Muzika et al., 2004). Climate warming might have had the additional effect of the increase in this phytotoxic O3 effect on forest. Synergistic O3 effects with high temperature and moisture stress are well known (McLoughlin and Downing, 1996). However, the statement that the effect of O3 and drought might counterbalance

each other (Zierl, 2002) is more significant when investigating phytotoxic O3 effect on trees. Closed stomata protect foliage from the uptake of high O3 concentrations into the leaves, which is typical of periods characterized by high temperature and moisture stress. Most likely therefore, the O3 effect in northern latitudes (where moisture stress is less frequent) often leads to plants becoming more susceptible to injury than in southern areas, despite the increase in O3 concentrations from north to south (Matyssek and Innes, 1999; Karlsson et al., 2002; Paoletti, 2006). In the Mediterranean region of southern Europe, annual peak O3 concentrations most often occur in June and August, i.e. later than in northern latitudes (Vingarzan, 2004). In this case the highest ambient O3 levels coincide with the time that natural Mediterranean vegetation suffers the most water stress (Paoletti, 2005). Closed stomata protect plants from O3 flux into the leaves and from its phytotoxic effect. Such constitutional and induced

A. Augustaitis, A. Bytnerowicz / Environmental Pollution 155 (2008) 436e445

443

Table 3 Contribution of ambient ozone to the integrated impact of different environmental factors on residual of pine stems basal area increment Variables

Models, F(a,b) (3,98)

In the air SO2 P þ PNH4NO3

(3,98)

(3,98)

þ e e

In precipitation SO24 NHþ 4 NO-3

(4,97)

(4,97)

(2,99)

þ

þ

e e e e e

þ þ þ

þ

Precipitation Last year IX-XI XII-II Current year III-V VI-VIII

e e

Temperature Last year IX-XI XII-II Current year III-V VI-VIII 0.4 16.4 16.0 0.000

(8,93) e

e e

e e e

6.3 15.3 9.0 0.002

(4,97)

þ

Deposition SO24 NHþ 4 NO-3

r2, % r2* with O3 effect, % O3 effect (r2*- r2) % O3 significance: p<

(4,97)

2.5 19.4 16.9 0.000

18.5 27.2 8.7 0.001

0.7 23.9 23.2 0.000

0.2 14.4 14.2 0.000

e e

þ e

þ

þ e

þ

7.7 17.2 9.5 0.001

10.2 17.2 7.0 0.005

e

þ e

e 21.7 31.6 9.9 0.000

Individual impact of peak O3 concentration on stem basal area increment residual: r2¼13.3% and p<0.0002. F(a.b) - models identified by F - test symbol with degrees of freedom: a - of the predictor variables; b - of the observations (STATISTICA software); significance of variables (þ) when p<0.05 and (e) when p>0.05 in model.

abilities of trees to tolerate oxidative stress, as well as their acclimation and adaptation, are the key factors resulting in a lack of relationships between O3 exposure and effects on crown transparency and radial growth in this region (Ferretti et al., 2003; Paoletti, 2006; Paoletti et al., 2007). In northern Europe, in contrast to its southern part, peak O3 concentrations were detected in April and early May; however, stomatal activity, and thus O3 uptake, were still low due to the soil being frozen at this time (Utrainen and Holopainen, 2000). Therefore, the most suitable regions in Europe to assess the effect of ambient O3 on forests could be its central and northeastern parts. In these regions, peak O3 concentrations in spring time coincide with the beginning of the period when natural vegetation does not suffer moisture stress (April and May). The predicted climate warming should increase the relevance of this problem in this region. Due to the growing season beginning up to 15 days earlier, compared to historic conditions, forests will become more sensitive to injury from ambient O3. The findings of this study revealed that the contribution of peak O3 concentrations to the integrated impact of the other environmental factors on Scots pine defoliation and basal growth increment remain statistically significant, confirming results obtained in Finland (Utrainen and Holopainen, 2000) and the Carpathian forest (Muzika et al., 2004). Also, the effects of peak O3

concentrations have higher significance for spruce trees in Norway than the mean diurnal O3 concentration or the AOT40 index in southern Sweden (Karlsson et al., 2006). Therefore, it seems that peak O3 concentration is one of the key factors affecting forest ecosystems in northeastern and northern Europe. The AOT40 index has been demonstrated to both overestimate and underestimate O3 phytotoxic risk in southern and northern Europe, respectively (Wieser and Tausz, 2007). Obtained data revealed that relationships between the AOT40 index and considered components of biota are insignificant or less significant than between the peak O3 concentrations and different components of forest biota. Different meteorological conditions and different acclimation and adaptation potentials of natural vegetation to O3 exposure could be the key factors in the controversial and unreliable estimation of O3 risk. Clearly there is a need for a scientifically sound O3 index addressing its phytotoxic potential in the European and northern hemisphere forests. Recent findings clearly show that O3 exposure does not adequately characterize the potential for plant injury, because plant response is more closely related to the amount of O3 absorbed into leaf tissue and modified by detoxification processes (effective flux) (Matyssek et al., 2007). Newly developed concepts based on O3 flux into leaves require profound knowledge of physiological processes, e.g. of both stomatal functioning,

444

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which determines stress avoidance through the degree of opening, and of stress tolerance, which is determined by structural and physiological leaf differentiation and related capacities in primary and secondary metabolism (Paoletti et al., 2007). Therefore, a well-coordinated and enhanced international cooperation in various disciplines such as atmospheric chemistry, forestry, botany, entomology, soil science, and dendrochronology in various regions of Europe is recommended. Since climatic changes in the Baltic region manifest themselves by the earlier (up to 15 days) beginning of the growing season, when the levels of O3 are high and plants have high stomatal conductance, a potential for phytotoxicity is much higher than in other parts of Europe where levels of ambient O3 are higher, but frequently occurring droughts may prevent plants from taking up high levels of O3, thus reducing the risk of severe phytotoxic effects (Ferretti et al., 2007; Paoletti, 2006; Paoletti et al., 2007). In this context the Baltic region seems to be the new and relevant European region for future studies on potential O3 phytotoxicity and the evaluation of risk to temperate forest ecosystems. 5. Conclusions In the Lithuanian forests, peak ambient O3 concentration is the key factor resulting in Scots pine growth reduction, while the key factors resulting in its defoliation seem to be air acidifying compounds and their deposition (O3 only predisposes these effects). However, when the effect of air acidifying compounds, their deposition and climatic factors was accounted for, the contribution of peak concentrations of ambient O3 to pine defoliation changes remained significant ( p < 0.05). The effect of the AOT40 index on the considered response variables was distinctly lower. Further investigations, including physiological studies, are needed to confirm our findings. Such investigations would help to better understand the O3 effect and the contribution of the O3 peak values to the changes in tree defoliation and growth under field conditions. This is especially true for the central and northeastern European forests, where the dehardening of forest trees due to climate warming will accelerate and consequently plant sensitivity to the effects of the spring-time peak O3 concentrations will increase. Acknowledgements Thanks are due to Dr Almantas Kliucius from the Lithuanian University of Agriculture for the help in the forest. We thank Dr Rasele Girgzdiene and Dr Dalia Sopauskiene from the Institute of Physics for providing data on environmental pollution. The authors also thank Ingrida Augustaitiene who helped prepare the manuscript. References Augustaitis, A., Juknys, R., Kliucius, A., Augustaitiene, I., 2003. The changes of Scots pine (Pinus sylvestris L.) tree stem and crown increment under decreased environmental pollution. Ekologia (Bratislava) 22 (1), 30e36. Augustaitis, A., Augustaitiene, A., Kliucius, A., Bartkevicius, E., Mozgeris, G., Sopauskiene, D., Eitminaviciute, I., Arbaciauskas, K., Mazeikyte, R., Bauziene, I., 2005. Impact of acidity components in the air and their deposition on biota in forest ecosystems. Baltic Forestry 2, 84e93.

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