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. 2003 Apr;91(5):559–569. doi: 10.1093/aob/mcg052

Influence of Elevated CO2 and O3 on Betula pendula Roth Crown Structure

OLEVI KULL 1,2, INGMAR TULVA 1,2, ELINA VAPAAVUORI 3
PMCID: PMC4242242  PMID: 12646500

Abstract

Elevated CO2 and ozone effects were studied singly and in combination on the crown structure of two Betula pendula clones. Measurements were made at the end of the second fumigation period in an open‐top‐chamber experiment with 9‐year‐old trees. Shoot ramification (number of long and short daughter shoots), shoot length, and number of metamers, leaves and buds were measured at four positions in every tree. As a result of increased temperature, trees in chambers had longer shoots and more frequent shoot ramification than control trees not enclosed in chambers. Ozone treatment decreased shoot ramification significantly. Additionally, ozone treatment resulted in an increased number of metamers in one clone. There was no statistically significant interaction between ozone effect and crown position; however, there was a slight tendency for the lower crown to be more affected by ozone. Elevated CO2 caused a significant increase in the number of long‐shoot metamers. Therefore, 2× ambient CO2 concentration partly ameliorated the negative effect of ozone because the increased number of leaves per shoot counteracted the decreased branching. Although the main effects of elevated ozone and CO2 were similar in the two clones, slight, statistically insignificant, differences appeared in their responses when interactions with crown position were considered.

Key words: Betula pendula Roth, silver birch, ozone, CO2, open‐top chambers, clones, shoot growth, ramification, metamers, crown structure, shoot dimorphism, sylleptic shoots

INTRODUCTION

Increased atmospheric CO2 and ozone concentrations are of concern because of their effects on forests. Many studies, mainly involving tree seedlings, have shown the potential of these trace gases to influence physiological processes and allocation of growth in trees. Saplings and larger trees have been studied less often because of technical problems and the high cost of manipulating large gaseous environments.

Tree structure is intrinsically coupled with function (Valladares, 1999). For instance, the role of canopy architecture in capturing light has been emphasized in many studies (Horn, 1971; Schulze et al., 1986; Ackerly and Bazzaz, 1995). Additionally, the existence of the biomechanical constraints of structure and the link between water transport and branching architecture have been shown often (Ford, 1985; Schulze et al., 1986; Valladares, 1999).

Trees show considerable plasticity in their structural properties (Halle et al., 1978). This plasticity gives a basis to the interpretation that trees actively grow towards the light resource (Schulze et al., 1986; Caldwell, 1987; Stoll and Schmid, 1998). Structural properties such as branching pattern, shoot length, and leaf number and size, are shown to be dependent on the local radiation climate. However, species vary greatly in these responses and, as a result of this diversity, a generalization has been proposed that links tree crown structure with light demand of the species (Boojh and Ramakrishnan, 1982; Fisher, 1986).

Light‐dependent changes in shoot growth and ramification affect the vertical distribution of foliage and also the total leaf area index (LAI) in a canopy (Kull et al., 1999). Sensitivity analysis of the canopy growth model showed that, besides the radiation model and its parameters, the most important growth‐related quantity that influences the canopy‐level steady‐state LAI is the shoot ramification ratio (a measure of the number of daughter shoots produced by the average shoot). Especially important in that respect is the shape of the relationship between the shoot ramification ratio and local photosynthetic photon flux density (PPFD). If the shoot ramification ratio is greater than one, then following every next bud‐break the number of shoots in that canopy region will increase and the tree crown expands, whereas in the degrading zone of the crown, the ramification ratio is below one. Because of a strong feedback between leaf area and radiation climate within a canopy, the PPFD value at which shoot ramification drops below unity predicts strongly the maximal LAI of the canopy. The model by Kull and Tulva (2000), developed for aspen, allows predictions to made about the canopy level from measurements of shoot parameters at the single tree level.

The effect of changes in CO2 or O3 concentration on tree growth has been documented in many studies. However, more data are available for small seedlings and total above‐ground biomass or growth than for larger trees or the distribution of a growth pattern within a tree crown (Sandermann et al., 1997; Pritchard et al., 1999; Bortier et al., 2000a). Carbon dioxide serves as the substrate for photosynthesis and therefore concentration changes usually have a direct effect on photosynthetic production and growth. Changes in the root : shoot ratio are often reported (Ceulemans and Mousseau, 1994; Saxe et al., 1998). In contrast, ozone is a strong oxidant and an increase in its concentration adds substantially to the oxidative power of the environment to which the plants are exposed. Therefore, the effect of ozone on growth is usually negative (Matyssek et al., 1992; Karnosky et al., 1996; Bortier et al., 1997; Kellomäki and Wang, 1998; Volin et al., 1998; Oksanen and Saleem, 1999). However, in several experiments the effect of ozone on growth has been negligible (Samuelson et al., 1996; Pääkkönen et al., 1998a), or has been overshadowed by the influence of other environmental factors, such as drought and shading (Pääkkönen et al., 1998b; Paludan‐Müller et al., 1999; Topa et al., 2001). Results of studies in which the interaction between CO2 and ozone fumigation on trees has been evaluated are diverse. It seems reasonable to expect that the damage caused by ozone is ameliorated by CO2 (Allen, 1990; Karnosky et al., 2001). Such an amelioration does often (e.g. Volin et al., 1998; Grams et al., 1999; Lütz et al., 2000), but not always (Barnes et al., 1995; Kull et al., 1996; Kytöviita et al., 1999) occur.

Although shoot growth responses to elevated CO2 and/or O3 have been studied (Matyssek et al., 1992; Norby et al., 1995; Chen et al., 1997; Barton and Jarvis, 1999; Broadmeadow and Jackson, 2000; Dickson et al., 2001; Isebrands et al., 2001), little is known about how manipulations of the gaseous environment of trees influence the pattern of shoot growth in different crown positions. Such information would allow us to make predictions on canopy level changes in response to changes in the global climate.

The main aim of this study was to evaluate the influence of elevated CO2 and O3 on the shoot growth pattern with respect to crown position in silver birch. The two silver birch clones used, originating from different parts of Finland, had been shown to differ in their response to ozone in a previous pot experiment (Pääkkönen et al., 1997).

MATERIALS AND METHODS

Trees and experimental design

Two fast‐growing clones of silver birch (Betula pendula Roth), one originating from southern Finland (Valkeakoski, 61°08′N, 28°48′E; clone 80 = K1659 in the Finnish forest genetic register) and the other from eastern Finland (Eno, 62°48′N, 30°05′E; clone 4 = V5952 in the Finnish forest genetic register), were selected. According to the results of a previous pot experiment, clone 80 was more sensitive to ozone than clone 4, assessed by an integrated ranking score based on visible leaf injury, leaf area and shoot dry weight of the seedlings at the end of the experiment (Pääkkönen et al., 1997). Saplings of these selected clones, grown in the field since 1993, were enclosed in open‐top chambers at the Suonenjoki Research Station, Finland (62°40′N, 27°00′E) at the beginning of 1999. The experimental design and performance of the fumigation system has been described in detail by Vapaavuori et al. (2002). The notional treatments were (1) chamberless control; (2) chamber control; (3) 720 ppm CO2 (24 h day–1); (4) doubled background O3 (between 0800 and 2000 h); and (5) 720 ppm CO2 + doubled background O3. In reality, in 1999, the CO2 concentration was between 675 and 725 ppm during 15 % of the exposure time and for 45 % of the time was between 625 and 775 ppm. During the growing season of 2000 the CO2 concentration was between 675 and 725 ppm for 38 % of the exposure time and between 625 and 755 ppm for 77 % of the exposure time. The background level of ozone in Suonenjoki is low (for 40 % of the daytime hours the ozone concentration of the ambient air was about 30 ppb maximum, although values of 45–55 ppb were occasionally recorded on sunny days during the late afternoon). In 1999, the elevated ozone treatment started in week 22 and in 2000 in week 19. Ozone concentration in the treatment was about 50 ppb during 20–21 % of the exposure time, and peak values of 100 ppb were recorded during 1·5 % of the exposure time. In the ozone treatment the AOT40 value (accumulated over the threshold of 40 ppb) was 18 ppm h greater in 1999 and 22 ppm h greater in 2000 than in ambient air, which is twice the currently set critical dose of 10 ppm h based on the observed 10 % growth decline of beech (Braun and Fluckiger, 1995; Fuhrer et al., 1997).

The mean daily temperatures in chambers were 2·3–2·7 °C higher than outside conditions, leading to a 400 degree‐days higher cumulative temperature sum in the chambers during the growing season of 2000 (Vapaavuori et al., 2002).

Both clones were represented as four replicates, resulting in 32 trees being enclosed in chambers and eight trees serving as outside controls. The fumigation started in May 1999 and the measurements reported here were made in August 2000, at the end of the second season of treatment. Trees were 5–8 m tall when the measurements were made.

Shoot growth measurements

Shoot ramification, shoot length and number of leaves and buds were counted at four positions in every tree. In the top of the tree the terminal shoot of the previous year (= main trunk) and all shoots grown on it during the previous year (= sylleptic shoots) and the current year were measured (Fig. 1). A 2‐year‐old lateral branch below the top was chosen as the second position. In the lower crown two branches were chosen as the third and the fourth branch positions, one at the height of 1·5–2·5 m and the other amongst the lowest living branches (approx. 0·5 m from ground). Light conditions at sample locations were measured using the hemispherical photography technique, with a Nikon CoolPix 900 digital camera equipped with hemispheric lens. Photographs of the upper hemisphere taken at sample locations were processed using WinScanopy Pro sofware (Regent Instruments Inc., Quebec, Canada). Calculated mean relative irradiance at sampled branches is given in Table 1. In the lower crown, where every shoot produces only a few new shoots and where local variability in light conditions was relatively large, all current and previous year shoots were measured in one first‐order lateral branch to get a well‐defined sample. Betula pendula is a species with shoot dimorphism. In short shoots, terminal bud‐set occurs shortly after the bud‐break and development of two or three leaves, so that only the first internode elongates to any extent. In long shoots, after the appearance of the first two leaves, the terminal meristem continues to produce new metamers with elongated internodes. In the present study, elongation of long shoots terminated in August with the formation of terminal buds. During the reported measurements in the second half of August 2000, all terminal buds, with very few exceptions, were set. An elementary unit of a shoot is defined as a metamer (Valladares, 1999). Every metamer consisted of an internode and a leaf and, in most cases, also an overwintering new bud (Fig. 1). Shoot length, number of metamers and buds were recorded in all selected shoots. All these measurements were carried out shoot by shoot, starting with a 3‐year‐old shoot. The notation protocol was such that it was possible to derive the number of daughter shoots for every previous‐year shoot. The average shoot ramification ratio was calculated as the average number of daughters per previous‐year shoot at each height level. Sylleptic shoots (Fig. 1), which are produced from current‐year buds, were counted separately.

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Fig. 1. Schematic presentation of the top of a birch tree explaining used terminology. CT, current year terminal; LT, last year terminal; CSL, current year sylleptic long shoot; CPL, current year proleptic long shoot; LSL, last year sylleptic long shoot; CS, current year short shoot. A metamer is a unitary part of a shoot consisting of a leaf, an internode and, in most cases, a bud.

Table 1.

Average relative irradiances at sampled branch positions measured from hemispherical photographs (irradiance at the open site equals 1)

Relative irradiance
Sample location Mean s.d.
Top 0·91 0·08
Upper lateral 0·72 0·11
Middle lateral 0·48 0·15
Lower lateral 0·32 0·14
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Statistical analysis

Data were analysed using the multi‐factor repeated measures ANOVA procedure of STATISTICA software package (StatSoft Inc., Tulsa, OK, USA). Dependent variables (shoot length, shoot ramification ratio, number of metamers, etc.) were the means of each height level with four trees as replicates. To achieve homogeneous variance and normal distribution of residuals, data on shoot and metamer length and number of metamers were square root transformed, while data on ramification were log‐transformed and proportions of sylleptic and long shoots were logit‐transformed {log[x/(1 – x)]}. In the evaluation of the chamber effect only data from control trees were used, with chamber and clone as independent factors and branch position as the within subject factor. In the evaluation of treatment effects, only chamber trees were used, with clone, CO2 level and ozone level as independent factors and branch position as the within subject factor.

RESULTS

Differences between clones and chamber effect

All measured shoot parameters declined significantly from top to bottom in the canopy (Figs 2 and 3; Table 2). In control trees, substantial differences appeared between clones in the proportion of sylleptic shoots produced and in internode length (Table 2). In the top of outside control trees, the proportion of sylleptic shoots was 28 % in clone 4 and 20 % in clone 80, and this difference increased considerably due to a chamber effect (41 % in the top of clone 4 versus 7 % in clone 80). The other significant difference between clones was in internode length (Table 2), which was substantially longer in lower branches of clone 80 (Fig. 2). Since the number of metamers was similar in the two clones, the difference in internode length converted also into the difference in shoot length (Fig. 2; Table 2).

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Fig. 2. Long shoot length (upper row), number of metamers (middle row) and internode length (lower row) in ozone tolerant clone 4 (left) and in ozone sensitive clone 80 (right) of Betula pendula as function of crown position. Filled circles, outside control trees; open squares, chamber control trees. Standard errors of estimate (n = 4) are shown with the error bars.

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Fig. 3. Total ramification (number of daughter long and short shoots) of long shoots (upper row) and proportion of daughter long shoots (lower row) in Betula pendula as a function of crown position. Filled circles, outside control trees; open squares, chamber control trees. Standard errors of estimate (n = 4) are shown with the error bars.

Table 2.

Summary of the effects of clone, chamber and branch position on shoot growth and ramification parameters according to repeated measures ANOVA with branch position as within subject factor (only outside and chamber control trees are included)

Effect Long shoot length No. of metamers Internode length Total ramification Proportion of sylleptic shoots† Proportion of long shoots
1 * n.s. ** n.s. ** n.s.
2 * n.s. n.s. * n.s. n.s.
3 *** *** *** *** – ***
1,2 n.s. n.s. n.s. n.s. n.s. n.s.
1,3 n.s. n.s. n.s. n.s. – n.s.
2,3 ** *** n.s. n.s. – n.s.
1,2,3 n.s. n.s. n.s. n.s. – n.s.
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Effects: 1, clone; 2, chamber; 3, branch position.

***, P < 0·01; **, P < 0·05; *, P < 0·1; n.s., P > 0·1.

† Only the topmost position is taken into the analysis.

The chamber effect was evident on shoot length and ramification (Table 2). In chambers, long shoots were longer in upper positions and slightly shorter in the lowest branches than in control trees not enclosed in chambers (Fig. 2).This was more due to changes in the number of metamers, although in both clones also the internodes were slightly longer in the upper positions of the crown (Fig. 2). The chamber effect was also significant for shoot ramification (Table 2). This resulted partly from the increased number of long shoots (Fig. 3). In general, the chamber effect on shoot ramification was complex: chambers causing an increase in ramification in the top of crowns in clone 4, whereas in clone 80, branching increased relatively more in the lower canopy (Fig. 3).

Fumigation effects

Ozone treatment affected shoot length (Fig. 4). However, this was statistically significant only with interaction with clone (Table 3). This is so because in clone 4, shoot length decreased in the lower positions of the crown, although only under elevated CO2, whereas in clone 80, ozone increased shoot length in these positions (Fig. 4). These ozone‐induced changes in long‐shoot length were due to similar changes both in the internode length and number of metamers (Fig. 4; Table 3). Ozone also caused an overall statistically significant decrease in total shoot ramification (Table 3). This decrease was more pronounced in clone 80 at ambient CO2 (Fig. 5). At elevated CO2, this negative effect of ozone almost disappeared (Fig. 5). However, all interactions of ozone with other factors (CO2, clone, branch position) remained statistically insignificant (Table 3).

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Fig. 4. Long shoot length (upper row), number of metamers (middle row) and internode length (lower row) in ozone tolerant clone 4 (left) and in ozone sensitive clone 80 (right) of Betula pendula as function of crown position. Filled circles, ambient O3 concentration; open squares, 2 × ambient O3 concentration. Standard errors of estimate (n = 4) are shown with the error bars.

Table 3.

Summary of the effects of clone, treatments and branch position on shoot growth and ramification parameters according to repeated measures ANOVA with branch position as within subject factor

Effect Long shoot length Number of metamers Internode length Total ramification Proportion of sylleptic shoots† Proportion of long shoots
1 *** n.s. *** n.s. *** n.s.
2 n.s. * n.s. n.s. n.s. n.s.
3 n.s. n.s. n.s. * n.s. n.s.
4 *** *** *** *** – ***
12 n.s. * n.s. n.s. n.s. n.s.
13 ** ** ** n.s. n.s. n.s.
23 n.s. n.s. n.s. n.s. n.s. n.s.
14 n.s. ** n.s. n.s. – ***
24 ** *** n.s. n.s. – n.s.
34 n.s. n.s. n.s. n.s. – n.s.
123 n.s. n.s. n.s. n.s. n.s. n.s.
124 n.s. n.s. n.s. n.s. – n.s.
134 n.s. n.s. n.s. n.s. – n.s.
234 ** ** n.s. n.s. – n.s.
1234 n.s. n.s. n.s. n.s. – n.s.
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Effects: 1, clone; 2, CO2; 3, O3; 4, branch position.

***, P < 0·01; **, P < 0·05; *, P < 0·1; n.s., P > 0·1.

† Only the topmost position is taken into the analysis.

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Fig. 5. Total ramification (number of daughter long and short shoots) of long shoots (upper row) and proportion of daughter long shoots (lower row) in clone 4 (left) and clone 80 (right) of Betula pendula as the function of treatment and crown position. Filled circles, ambient O3 concentration; open squares, 2 × ambient O3 concentration. Standard errors of estimate (n = 4) are shown with the error bars.

Elevated CO2 affected most strongly the number of long‐shoot metamers (Table 3). Statistically significant influence of CO2 on the number of long‐shoot metamers also appeared in interactions with clone and canopy position (Table 3). This is because CO2 increased the number of metamers more in clone 4 than in clone 80 and more in the lowest crown position than in the upper crown (Fig. 4). Internode length was unaffected by elevated CO2 (Table 3). There was no statistically significant influence of elevated CO2 on shoot‐ramification‐related parameters (Table 3). However, in clone 80 there was a tendency for the proportion of long shoots to increase in the lower crown positions at elevated CO2 (Fig. 5).

The only statistically significant three‐way interaction appeared in CO2 × O3 × branch on the number of long shoot metamers (Table 3). The synergistic effect was expressed in the number of metamers of the uppermost lateral branch where this parameter decreased in O3 treatment and was not significantly affected by CO2 treatment alone. However, in the combination of O3 × CO2, the number of long‐shoot metamers increased (Fig. 6). Interestingly, this three‐way interaction appeared similarly in both clones, although in clone 4 the difference between the number of metamers in CO2 and CO2 + O3 treatments was not significant. Additionally, such a synergistic effect of combined CO2 and O3 did not appear in other crown positions.

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Fig. 6. Number of long shoot metamers in the upper lateral branches (crown position 2) where statistically significant synergetic effect of CO2 + O3 treatment appeared (Table 3). ChaControl, chamber control; O3, 2 × ambient O3 concentration; O3 + CO2, 2 × ambient O3 + 2 × ambient CO2; CO2, 2 × ambient CO2. Standard errors of estimate (n = 4) are shown with the error bars.

DISCUSSION

Chamber effect

Environmental factors strongly influenced shoot growth in birch. It has often been shown that branching and shoot length depend on light conditions (Valladares, 1999). In birch this light dependence seemed to be especially strong because shoot length and ramification declined substantially from the top to the bottom of the crown. This pattern differs from that in oak canopies Kull et al. (1999), where shoot ramification changes very little within most of the crown height and declines rapidly only at very low light intensities at the lowest part of the living crown. In the current study, some of the measured chamber effects may also be attributed to altered light conditions within the chambers. It is likely that because of reflectance from the chamber walls the vertical profile of PPFD is altered, especially during episodes of direct sunshine. This may partially explain the altered vertical pattern in the number of long shoots. However, temperature is most strongly affected in the chamber, resulting in 2·3–2·7 °C increases in the mean daily temperatures in the chambers compared with outside conditions. It is known that temperature strongly influences shoot growth, especially in species with indeterminate growth pattern. Often temperature affects shoot length because leaf initiation depends on temperature (Pieters et al., 1999). This is in accordance with our data since the chamber effect was stronger on the number of metamers than on the length of internodes (Table 2; Fig. 2). Increased shoot ramification may be explained also by a temperature effect because the increased number of metamers is accompanied by an increased number of buds and, additionally, temperature usually has a strong effect on bud development (Brown, 1971) causing changes in bud break.

Fumigation effects

Ozone is a strong oxidant, which in the plant environment often suppresses photosynthesis and the overall dry mass increment (Karnosky et al., 1996; Oksanen and Saleem, 1999). Although changes in the relative allocation to shoots and roots are often reported (Coleman et al., 1995; Oksanen and Saleem, 1999), only rarely has the influence of ozone on the branching pattern of trees been studied. Some investigators have reported decreased branching frequency in birch under treatment with ozone (Maurer and Matyssek, 1997; Matyssek et al., 1992), but unfortunately quantitative investigations are missing. In our experiment, exposure to ozone caused a statistically significant decrease in branching of both birch clones. Considerably more information is available about the effect of ozone on growth of branches or shoots. Shoot length has been found to increase or decrease under ozone fumigation (Gunthardt‐Goerg et al., 1993; Samuelson et al., 1996; Bortier et al., 2000a). This pattern also appeared in our study. In clone 4 mean shoot length decreased and in clone 80 it increased when averaged over all crown positions. Such a variable response may be explained by two opposite trends. Ozone reduces overall growth and accelerates leaf senescence, but sometimes new leaf initiation and, hence, number of metamers produced is increased to compensate for leaf loss (Bortier et al., 2000a). However, in several studies no such increase in leaf initiation has been detected (Karnosky et al., 1996; Bortier et al., 2000b). Although we did not monitor leaf loss, we did not find a differential influence of ozone on internode length and number of metamers, since both of these parameters changed in parallel to shoot length. In our experiment, no significant interaction was found between ozone and crown position on shoot growth. This is in accordance with several studies showing that neither the canopy position (Samuelson and Edwards, 1993), nor microclimate (Samuelson, 1994) had significant influence on the response of shoot growth to ozone. However, this contrasts with effects of ozone on photosynthesis or stomatal conductance, where these functions are often more impaired in the shaded conditions of the lower canopy (Tjoelker et al., 1995).

Being a substrate for photosynthesis, CO2 concentration strongly influences plant growth and allocation (Ceulemans and Mousseau, 1994; Saxe et al., 1998; Ward and Strain, 1999; Kerstiens, 2001). In our experiment shoot length was slightly increased, mainly because of the increased number of metamers, showing that leaf initiation was slightly accelerated. Several investigators have observed increased branching at elevated CO2 levels (Lawlor and Mitchell, 1991; Chen et al., 1997; Saxe et al., 1998). Our study showed that the change in the total number of daughter shoots was negligible, and increase in the appearance of long shoots was dependent on crown position. Additionally, we noticed some, though statistically insignificant, increase in sylleptic branching in clone 80, indicating that elevated CO2 might reduce apical dominance (Chen et al., 1997; Pritchard et al., 1999). Influence of CO2 on shoot growth was especially significant as an interaction with branch position. At least theoretically, elevated CO2 should enhance photosynthesis more in shade conditions of the lower crown compared with high light conditions at the top of the trees (McDonald et al., 1999; Norby et al., 1999). This may explain why, in the lower crown, relatively more long shoots were produced in clone 80 and more metamers formed in clone 4 under elevated CO2, since bud development and long shoot growth are directly related to photosynthetic production of leaves.

It has been hypothesized that fast‐growing tree species, which are usually shade intolerant and often show indeterminate shoot growth, should react rapidly to elevated CO2 because they can change sink strength in a flexible way (Poorter, 1993; Ward and Strain, 1999). However, this hypothesis has not been confirmed in all experiments (Saxe et al., 1998; Tjoelker et al., 1998; Kerstiens, 2001, but see Atkin et al., 1999 or Ward and Strain, 1999). Increased numbers of long shoots in the lower crown and a slight change in the number of long‐shoot metamers indicated some flexibility; in our experiment, however, these changes were clearly smaller than expected.

The main question that experiments with simultaneous fumigation with CO2 and O3 address is whether elevated CO2 can ameliorate the negative effect of O3 (Allen, 1990; Dickson et al., 1998; Poorter and Perez‐Soba, 2001). In addition, in some experiments, a synergistic effect of the O3 × CO2 interaction has been reported (Kull et al., 1996; Kytöviita et al., 1999). In the present study, O3 and CO2 influenced different shoot growth parameters. In spite of slight differences in the reactions of the two clones, the conclusion is that O3 decreased overall ramification, whereas CO2 increased leaf initiation and shoot growth. In that sense, CO2 ameliorated the negative effect of ozone. There was, at least in statistical terms, a significant interaction between O3, CO2 and branch position (Table 3). Ozone alone decreased the number of metamers at the uppermost lateral branch, whereas CO2 alone had no influence. However in the combined O3 + CO2 treatment, the number of metamers in this branch increased. Although this effect appeared, to some extent, in both clones, it is difficult to explain such behaviour. Nevertheless, it is reasonable to conclude that, as a consequence of the synergistic effect of CO2 and O3, vertical distribution of shoot growth was affected.

Genetic differences

The branching pattern of a tree depends on both genetic properties of an individual and environmental conditions. The first is most clearly seen if different species are compared: many distinct architectural models have been described (Valladares, 1999). However, evidence shows that varieties and genotypes may have substantially different branching patterns within species (Ford, 1985; Henry and Aarssen, 2001). In our study, the most important difference between the two clones was in sylleptic branching when only the outside control trees were compared. Sylleptic branching, the production of new shoots from current buds without an intervening rest period, is common within light‐demanding species with an indeterminate growth pattern and results in an excurrent crown form (Brown, 1971; Ford, 1985). This happens because weak apical dominance, which results in extensive sylleptic growth, is usually co‐occurring with strong apical control over proleptic shoots (Ford, 1985). Such an inter‐relationship between apical dominance and apical control was also seen in the present study. The strong apical dominance in clone 80 trees was accompanied by weak control over proleptic growth, since total ramification in the top crown was still higher than in clone 4 because of more proleptic shoots. Appearance of short shoots, which in some species is also related to apical dominance, (Ford, 1985) was not the case in birch, because short shoots in the trees in the present study, were never sylleptic. In the upper crown, short shoots usually emerged at the base of the previous‐year shoot and often also just above the previous‐year sylleptic branches. In the lower crown, production of short and long shoots seemed to be more related to the local light environment than to the position on the branch.

In the former pot experiment with the same clones, clone 80 was found to be more ozone sensitive than clone 4 (Pääkkönen et al., 1997). The current experiment with saplings does not support this grading unequivocally. Although ozone decreased the total ramification more in clone 80 than in clone 4 at ambient CO2, long‐shoot growth was enhanced in this clone under elevated ozone concentrations. Differences in the reactions of the clones between experiments may also be caused by different experimental conditions. Clone 80, originating from south of the experimental site in Suonenjoki, seemed to grow better in chamber conditions than clone 4, which originated from a similar latitude to Suonenjoki. This may mean that clone 80 was better adapted to warmer chamber conditions than clone 4 and reactions to additional ozone stress were equalized.

What can be expected at canopy level?

Norby et al. (1995) emphasized that in fumigation experiments with tree seedlings and saplings, a principal question about what will happen at the canopy level usually remains unanswered. Desirable canopy level information is related to possible changes in total LAI that the canopy can achieve, and changes in vertical distribution of leaf area density. Both parameters are important in predicting canopy level production (Jarvis, 1989; Norby et al., 1999). Using a sensitivity analysis of the canopy growth model, we have shown that the canopy steady‐state LAI is most strongly affected by changes in the long‐shoot ramification pattern, with respect to the radiation profile within the canopy, as well as by the extent of spatial heterogeneity of the leaf area within the canopy (Kull et al., 1999; Kull and Tulva, 2000). Combining these findings with the results of the current study it seems that CO2 would enhance steady‐state LAI, because the light limit at which long shoots appear is likely to be shifted towards lower values. Additionally, this increase in steady‐state LAI is expected to be more pronounced in clone 80 because, in this clone, ramification also increased in response to elevated CO2 in the top of the trees. Increased sylleptic branching in the top of the trees will increase spatial clumping of the foliage in this clone, probably resulting in an altered vertical pattern of the leaf area density. Ozone influences in the present study were modest but if we were to extrapolate the findings to canopy level, the increased ozone concentration will most likely lead to decreased steady‐state LAI, without noticeable changes in vertical leaf area distribution.

ACKNOWLEDEMENTS

We thank E. Oksanen and an anonymous reviewer for many useful comments. This work was supported by grant ERB IC15 CT98 0102 from the European Commission and partially by grant 3775 from the Estonian Science Foundation.

Supplementary Material

Content Snapshot
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Received: 19 July 2002; Returned for revision: 4 October 2002; Accepted: 14 December 2002    Published electronically: 20 February 2003

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