SEARCH

SEARCH BY CITATION

Keywords:

  • elevated CO2;
  • competition;
  • free-air CO2 enrichment (FACE);
  • short rotation culture;
  • Populus;
  • growth

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • • 
    In a free-air CO2 enrichment (FACE) study, above-ground growth of Populus alba, Populus nigra and Populus×euramericana was followed continuously during the first rotation cycle of a short rotation culture (SRC) plantation to test possible changes in the response to elevated CO2 occurring from planting until canopy closure.
  • • 
    Height, stem basal area, stem volume index, branch production, and bud phenology were monitored for 3 yr. Moreover the coefficient of variation and a competition index were calculated to analyse the onset and the typology of competition.
  • • 
    Volume index was higher under elevated CO2 by 77%, 24% and 22%, as mean value for the three species, in the first, second and third years, respectively. The stimulating response, although univocal, differed in extent among species. Branch production was stimulated only in the first year, whereas bud phenology was unaffected.
  • • 
    The analysis of these results show that growth was stimulated by elevated CO2 only in the first year, although differences in volume index remained significant even in the second and third years. In the third year, under canopy closure, only competitively advantaged individuals profited by the FACE treatment.

Abbreviations
SRC

short rotation culture

PGP

permanent growth plot

H

stem height

D

stem basal diameter

D2H

stem volume index

AGR

absolute growth rate of D2H

RGR

relative growth rate

BA

basal area

HGI X

height growth increment of year X

BAI X

basal area increment of year X

RSBPR

relative sylleptic branches production rate

CI

competition index

COV

coefficient of variation

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Forests play a significant role in the global carbon cycle and in the control of carbon dioxide concentration in the atmosphere. They not only passively undergo global climatic changes but are also driving factors that may influence the course of climatic change. The scientific community has therefore sought to assess and quantify both the response and the contribution of forests (Dixon et al., 1994). Our current knowledge of tree responses to elevated atmospheric CO2 concentrations under different experimental conditions has been summarized in recent reviews (Eamus & Jarvis, 1989; Ceulemans & Mousseau, 1994; Jarvis, 1998; Saxe et al., 1998; Norby et al., 1999). Almost all experiments demonstrated that tree growth – quantified in terms of stem height, total biomass or leaf area development – increased under enhanced levels of CO2 concentration. Elevated CO2 also stimulated biomass production of plants with indeterminate growth more than for plants with determinate growth, presumably because of differences in sink strength (Oechel & Strain, 1985). As stem growth and standing biomass are the most obvious indications of the performance of a forest ecosystem, above-ground growth has primarily been used to quantify the response of forests to global change (Norby et al., 1999).

The Free-Air CO2 Enrichment (FACE) technology has been developed to treat and examine entire ecosystems while minimizing the environmental disturbance between the CO2-treated and the surrounding ‘control’ plant communities (Hendrey et al., 1993; Norby et al., 1999).

As in other forestry FACE studies (DeLucia et al., 1999; Dickson et al., 2000; Norby et al., 2001), the enriched treatment at POPFACE provided a CO2 concentration of 550 ppm, representing the expected atmospheric CO2 concentration near the middle of this century (Schimel et al., 1996).

Poplar was chosen for this experiment in order to quantify the carbon sequestration capacity of an intensively managed tree plantation with potential as a partial sink for surplus, man-made CO2 emissions. Poplars are the most promising trees for short rotation cultures (SRC), a kind of agro-forestry system in which trees are intensively managed with the aim of maximizing biomass production for pulp, timber or energy (Beaton et al., 1991; Galinski et al., 1991; Ceulemans et al., 1992). A number of studies have been carried out on the effects of elevated atmospheric CO2 on Populus (Radoglou & Jarvis, 1990; Bosac et al., 1995; Ceulemans et al., 1995; Curtis et al., 1995; Gardner et al., 1995; Pregitzer et al., 1995; Kalina & Ceulemans, 1997; Tognetti et al., 1999), but all of them had a limited duration of treatment and were performed on individual or isolated plants except for the Aspen FACE experiment on Populus tremuloides (Isebrands et al., 2001; King et al., 2001). Before now there have been very few manipulative experiments where tree growth has been studied until the closed-canopy stage (Norby et al., 1999; Norby et al., 2001). In the present experiment growth dynamics were followed during three growing seasons, from planting until canopy closure, i.e. with LAI values from 0 until about 8 (Gielen et al., 2003).

Because growth was initially stimulated by FACE (Calfapietra et al., 2001), competition may differ between control and FACE treatments, and some assumptions have been made about competition in our study (Gielen et al., 2001, 2002). Therefore, to understand the growth of a stand exposed to elevated CO2, particularly of a high-density plantation, information about the competition in the stand is strongly needed. Generally, two models of competition are supported in the literature, one-sided (asymmetric) competition and two-sided competition (symmetric or asymmetric) (Perry, 1985; Weiner, 1985, 1986; Toméet al., 1994). When competition is one-sided, larger trees obtain a disproportionate part of resources and suppress the growth of smaller individuals, whereas the term two-sided competition is used when resources are shared equally or in proportion to size (Soares & Tomé, 1996). An important hypothesis relates one-sided competition to competition for light, and two-sided competition to the use of water and/or nutrients (Weiner, 1986; Soares & Tomé, 1996).

At the POPFACE experiment a complete harvest was carried out after 3 yr of enrichment, i.e. at the end of the first rotation cycle, evidencing a significant stimulation of total biomass in FACE treatment (Calfapietra et al., 2003). Given that, the objective of the present research was to study the above-ground growth dynamics throughout the first 3 yr of CO2 enrichment at the POPFACE experiment to understand whether the stimulation under elevated CO2 changed with time and in particular if it was also sustained after canopy closure. The second objective was to study whether this response in poplar was species-specific.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Site description

The experimental plantation and FACE facility were located in an agricultural region of central Italy, near Viterbo (Tuscania; 42°22′ N, 11°48′ E, alt. 150 m). The experimental site was only 15 km from the coast so that wind conditions were favourable for the FACE design (Miglietta et al., 2001). In spring 1999, after a detailed soil analysis, six experimental areas (30 m × 30 m) further called ‘plots’ were selected within a 9-ha field. Three of these areas, representing the ‘control’, were left untreated. In each of the other three plots representing the ‘FACE’ treatment, a PVC ring (22 m diameter) mounted on telescopic poles was established. In order to avoid cross contamination between FACE and control, the minimum distance between plots was 120 m. Pure CO2 was released through laser-drilled holes in the PVC ring. Meteorological information, used to control the release of CO2, was obtained from an automatic monitoring station located at the centre of each plot. Directional release of gas along the ring was controlled by shut-off valves located before the point of injection. The released quantity of gas was established, according to wind speed, using an algorithm developed for the facility and based on a 3-D gas dispersion model. The mean CO2 concentration was 544 ± 48 ppm during the first year of treatment, 532 ± 83 ppm during the second year and 554 ± 95 ppm during the third year, within the treated plots. Due to unexpected internal corrosion of the CO2 bulk container, performance problems occurred in the autumn of the second year. However, the CO2 concentrations measured at 1-min intervals at the centre of the FACE plots and at the top of the canopy were for more than 80% of time within 20% deviation from the pre-set target. The CO2 concentrations at different points within the plots were monitored for short periods throughout the season by two additional portable infra-red gas analysers connected to a multiport sampler. Despite larger short-term CO2, fluctuations were observed in the canopy space, the mean daily values only slightly differed from those measured at the top of the canopy (F. Miglietta, unpublished data). Daytime CO2 enrichment was provided from bud burst to leaf fall. A detailed description of the set-up and performance of this FACE facility was given by Miglietta et al. (2001).

Plant material and plantation layout

The poplar plantation was established in June 1999 using uniform hardwood cuttings (length 25 cm). The entire 9-ha field was planted with Populus×euramericana Dode (Guinier) (= Populus deltoides Bart. ex Marsh. × Populus nigra L.) genotype I-214 at a planting density of 5000 trees ha−1 (spacing 2 m × 1 m). The six experimental plots were planted with three different poplar species at a planting density of 10 000 trees ha−1 (spacing 1 m × 1 m) in order to have a sufficient number of experimental trees and a closed canopy after a short time. This planting density is common in SRC poplar plantations (Friend et al., 1991; Hansen, 1991; MacPherson, 1995; Tognetti et al., 1999). The three species were the hybrid Populus×euramericana Dode (Guinier) (genotype I-214), Populus nigra L. (genotype Jean Pourtet) and a local selection of Populus alba L. (genotype 2AS11). Further information on these species is contained in Calfapietra et al. (2001). Each plot was divided into two parts by a physical resin-glass barrier (1 m deep in the soil) for planned nitrogen treatments in the two halves of each plot, although no nitrogen treatments were applied during the first 3 yr of the experiment. Each half plot was further divided into three sectors, each occupied by a different species.

Before planting, cuttings of P. alba were treated with a phytohormone (IBA, 2000 ppm) to stimulate the formation of roots, notoriously difficult in this species. Additional cuttings were planted in pots filled with the site soil to obtain a sufficient number of plants for possible replacements. Rooting of P. nigra and P. × euramericana was very successful (99%). For P. alba, a partial replacement (about 30%) was necessary in the first weeks following planting using plants raised in the greenhouse.

A drip irrigation system was installed both in the field and in the experimental plots to avoid drought stress during the initial establishment phase and during the very dry summer period. Irrigation was monitored to ensure equal applications in each experimental plot. The amount of water supplied to trees increased from spring to summer and from the first to the third year in accordance with increased tree transpiration, reaching values of 10 mm d−1 in the summer of the third year.

At the beginning of the second year scaffolds were placed near the experimental trees in order to reach the top of the canopy. Weeds were removed manually or mechanically. A limited use of insecticides was unavoidable during the establishment year. Further information is contained in Scarascia-Mugnozza et al. (2000).

Growth measurements

Nondestructive growth measurements were carried out for 3 yr starting from August 1999 until the end of November 2001. Stem height (H) and basal stem diameter (D) were measured every 2 wk during the first two growing seasons and every month during the third growing season on a sample of six adjacent trees selected within each sector of the experimental plots. Consequently, there were six experimental groups per plot, each of these including six trees. Each group of six adjacent trees, surrounded by at least one row of the same species (to avoid possible border effects), represented the ‘Permanent Growth Plot’ (PGP) which was left undisturbed throughout the course of the experiment. Since no nitrogen treatment was applied in the two halves of each plot, all growth characteristics were measured on a sample of 12 trees per species in each plot.

Stem diameter measurements were made using a digital calliper (Mitutoyo, type CD-15DC, Andover, UK) at 20 cm above the soil as recommended by Pontailler et al. (1997). A graduated height pole was used for stem height measurements. At the end of each growing season, the stem height and basal diameter of 48 trees (including all PGP trees and those surrounding them) per species per plot were measured to verify whether the PGPs were representative of the entire population.

Stem basal area (BA) was calculated from values of basal diameter. Using basal diameter (D) and height (H) measurements, the stem volume index was calculated as D2H. Given the lack of biomass samplings in the first part of the growing cycle, this index was chosen as the main parameter to analyse the effect of elevated CO2 on growth dynamics. In fact, D2H is usually well correlated with above-ground biomass (Madgwick, 1971; Verwijst, 1991; Pontailler et al., 1997; Scarascia-Mugnozza et al., 1997) and this was especially true in our case with the r2 ranging from 0.942 to 0.964 according to the species. Moreover, taper index calculated as 1 − A4/A1.3 (where Ax is the cross-sectional area at height x, Norby et al., 2001) and wood density (Calfapietra et al., 2003) did not change between treatments.

Basal area increment (BAI) and height growth increment (HGI) were calculated for the second (BAI 2, HGI 2) and the third years (BAI 3, HGI 3) from end-year values.

Absolute growth rate (AGR) and relative growth rate (RGR) were calculated according to Hunt (1982) and as used for stem volume index values by Ceulemans & Deraedt (1999). AGR was calculated for D2H whereas RGR was calculated both for BA and D2H from end-year values and the length of each growing season described below. To disentangle CO2 responses and ontogeny, we examined the growth of trees of the same size but in different treatments, an approach proposed by Poorter (1993), Rey & Jarvis (1997) and Centritto et al. (1999). An analysis of covariance was performed for AGR of individual trees and their corresponding initial D2H values (covariate) during a 4-wk period in the first part of each growing season.

Competition

Typically, stand variability is investigated using the skewness of the tree size distribution, but coefficients of size inequality (e.g. coefficient of variation, COV) were suggested to be more valuable in the absence of density-dependent mortality (Weiner, 1986). Therefore, we calculated COV for BA at the end of the first, second, and third years. Additionally, RGR of BA in the second and third years was plotted against tree BA, and a correlation coefficient calculated (Perry, 1985; Soares & Tomé, 1996). Stem diameters of all trees (n = 48 per species per plot excluding border trees) were used in these analyses. In the third year, Hegyi's competition index (CI) was calculated as it was reported to perform well for tree species (Tomé & Burkhart, 1989; Holmes & Reed, 1991; Piutti & Cescatti, 1997). Hegyi's CI of eight experimental trees for each species was computed in all plots (Hegyi, 1974):inline image

where DBH is stem diameter at 130 cm of the ith subject (si) and the jth competitor (cj), respectively, and Lij the subject-competitor distance. Competitors were 8 trees of the square surrounding the subject tree, i.e. 4 trees at 1 m and 4 trees at 1.4 m distance. Values of trees surrounded by at least one dead or damaged tree were discarded. Trees were categorized by CI in 4 competition classes merging values from the three species and the differences between treatments analysed. An analysis of covariance was performed for RGR of BA of individual trees of the three species and their corresponding CI (covariate) in the third year.

Branches

Sylleptic branches are defined as branches that develop from axillary buds not undergoing a rest period (Remphrey & Powell, 1985). During the first growing season, sylleptic branches on the main stem were counted every 2 or 3 wk on the PGP trees. During the second and the third growing seasons, new sylleptic branches produced on the main stem were counted on a sample of four trees per species per plot because of difficulties in reaching the highest part of the canopy.

Based on the length of the growing season and the stem length produced per growing season (HGI), the Relative Sylleptic Branch Production Rate (RSBPR) was calculated for each species and in each treatment as the number of sylleptic branches produced per day and per unit of stem HGI [m]. The RSBPR allowed standardization of branch production to tree size and to growing season length, which differed considerably among species.

Proleptic branches are defined as those originating from buds that have undergone a winter rest period. At the beginning of the second and the third growing seasons, newly produced proleptic branches on the main stem were counted on four trees per species per plot. The number of (proleptic) branches per unit of stem HGI was obtained.

At the end of the first and the second years, diameters of all branches present on the main stem were measured on four trees per species per plot and their BA calculated. Diameters were measured on the branches at approximately 2 cm from their insertion on the stem to avoid possible basal enlargements. In the first year, only sylleptic branches were present. Three types of branches were present in the second year: sylleptic branches produced in the first year on HGI 1, sylleptic branches produced in the second year on HGI 2, and proleptic branches originated, by definition, on HGI 1. The ratio of stem BA to branch BA was obtained.

Bud phenology

Visual observations of the buds on the main stem were made every 2 or 3 d from the end of August until the end of October during each growing season. The date of bud set was determined by visual inspection of apical bud formation. All phenological observations were carried out on all PGP trees (12) per species per plot and mean dates (± se) were calculated.

1 July was considered as the beginning of the first growing season, coincident with the onset of shoot extension. At the beginning of the second and the third growing seasons, bud burst of PGP trees was determined by visual observations of the apical bud every 3 d from the middle of March until the middle of April. Stages of bud development and of bud opening were described as six classes from 0, completely closed to 5, leaves fully unfurled from the bud (Castellani et al., 1967). The length of the second and third growing seasons, expressed as number of days, was calculated from the dates of bud burst and bud set. Bud burst class 4 was the stage when shoot extension started.

Statistical analysis

To determine the main effects of FACE treatment and species on tree growth and branch production, an analysis of variance (anova) was carried out. Data were first tested for normality using the Shapiro-Wilk statistic (proc univariate in SAS). A randomized, complete-block design with treatment, species, and the treatment–species interaction as fixed factors, and block as random factor, was applied. Plot (3 control plots and 3 FACE plots) was the unit of replication. All statistical analyses (both anova for analysis of variance and ancova for analysis of covariance) were performed in SAS (SAS system 8.1, SAS Institute Inc., Cary, NC, USA) using the mixed procedure (Littell et al., 1996). Satterthwaite's procedure was applied to obtain the denominator degrees of freedom. Where the anovaF-test highlighted an interaction between treatment and species, a posteriori comparison of means was performed using estimates given by SAS. The Bonferroni method was used to correct for the multiple comparisons. Differences between means were considered significant when the P-value of the anova or the ancova test was < 0.05.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Growth

Stimulation of growth by elevated CO2 was evident a few weeks after planting, particularly for P. nigra and P. ×euramericana. As shown in Fig. 1a the slope of the curves of BA evolution increased considerably in the FACE treatment, resulting in BA difference between control and FACE by +96% for P. nigra, +64% for P. × euramericana and +26% for P. alba at the end of the first year. At that time, P. nigra had the largest BA, 2.54 cm2 in control and 4.97 cm2 in FACE (Table 1). P. alba was considerably smaller with BA values of 1.38 cm2 and 1.74 cm2 in control and FACE treatments, respectively. Height of all species was stimulated by about 10% at the end of the first year (Fig. 1b, Table 1). At the end of the second year, differences in height between treatments decreased and differences among species became negligible (Tables 1 and 2). An effect of FACE by about 20% was measured on BA in P. nigra and P. × euramericana. BA was equal in these species both in control and in FACE; smaller values and smaller CO2 effects were registered for P. alba. During the third year, differences in BA between treatments increased for P. alba and this same trend was observed for height in P. nigra and P. × euramericana.

image

Figure 1. Evolution of (a) stem basal area and (b) stem height during the first, second and third years for Populus alba (square), Populus nigra (triangle) and Populus × euramericana (circle) under control (open symbols) and FACE (closed symbols) treatments. Symbols represent the mean ± SE of 3 plots.

Download figure to PowerPoint

Table 1.  Values of the main parameters of stem growth (± SE) for three Populus species grown under control and free-air CO2 enrichment (FACE) treatments for 3 yr
 P. albaP. nigraP. × euramericana
Control FACEControl FACEControl FACE
  1. The effect of FACE (always positive) is indicated as ((FACE-control)/control)%. Each value represents the mean value of 3 plots. BA, basal area; BAI X, basal area increment of year X; HGI X, height growth increment of year X.

1st year
BA (cm2)1.38 (0.12)26%1.74 (0.13)2.54 (0.14) 96%4.97 (0.25)2.31 (0.19)64%3.79 (0.23)
Height (cm)140 (9) 9%152 (12)168 (5) 11%186 (5)141 (2)11%156 (5)
D2H (dm3)0.26 (0.08)38%0.36 (0.11)0.56 (0.05)121%1.24 (0.16)0.45 (0.03)73%0.78 (0.06)
2nd year
BA (cm2)13.96 (0.72)10%15.39 (0.65)20.39 (0.81) 21%24.60 (0.66)20.52 (1.24)20%24.64 (1.14)
Height (cm)557 (14) 8%602 (27)587 (8)  3%606 (6)576 (5) 3%592 (14)
D2H (dm3)10.09 (0.59)19%12.01 (1.43)15.22 (0.67) 27%19.28 (0.99)15.53 (1.12)25%19.45 (0.97)
BAI 2 (cm2)12.58 13.6517.85 19.6318.21 20.85
HGI 2 (cm)417 450419 420435 436
3rd year
BA (cm2)23.51 (1.40)13%26.64 (1.22)32.77 (1.60) 21%39.76 (1.37)30.99 (2.09)14%35.48 (1.76)
Height (cm)845 (10) 6%896 (20)873 (14)  6%928 (10)845 (12) 7%901 (15)
D2H (dm3)26.24 (1.10)20%31.11 (3.03)36.51 (1.19) 29%47.01 (2.14)34.67 (4.10)18%40.96 (1.82)
BAI 3 (cm2)9.55 11.2512.38 15.1610.47 10.84
HGI 3 (cm)288 294286 322269 309
Table 2.  Analysis of variance (ANOVA) of growth and production characteristics of three Populus species under control and free-air CO2 enrichment (FACE) treatments at the end of 3 yr
  TreatmentSpeciesTreat. x Species
  1. Significance (P-values of the ANOVAF-test) of the effects of CO2 treatment, species, and their interaction are indicated as *, P < 0.05; **, P < 0.01; ***, P < 0.001; ****, P < 0.0001. Values of P < 0.1 are also indicated. BA, basal area; RGR, relative growth rate of D2H; syll, sylleptic branches; prol, proleptic branches; RSBPR, relative sylleptic branches production rate.

1st yearBA**** 
Height*** 
D2H******
RGR (D2H)***** 
No. syll (HGI 1)< 0.1*****
RSBPR ****< 0.1
BA syll (HGI 1)*******
2nd yearBA***** 
Height   
D2H***** 
RGR (D2H)*** 
No. prol (HGI 1) * 
No. prol/unit lenght (HGI 1) ** 
No. syll (HGI 2) **** 
RSBPR **** 
BA syll (HGI 1)******
BA prol (HGI 1) ** 
BA syll (HGI 2) **** 
3rd yearBA**** 
Height*  
D2H*** 
RGR (D2H) ** 
No. prol (HGI 2) **** 
No. prol/unit lenght (HGI 2) **** 
No. syll (HGI 3) **** 
RSBPR *** 

Given that, the stem volume index D2H was considerably enhanced by the FACE treatment at the end of the first year, especially in P. nigra (+121%) and in P. × euramericana (+73%). This large stimulation of volume index by FACE progressively decreased during the second year (Fig. 2) converging for all species to a common value of approximately +20%. The larger values involved in second year calculations necessarily caused smaller relative differences between treatments, nevertheless percentage differences remained almost constant during the third year for all species. The different responses to FACE in the first and in the second years were confirmed by the analysis of RGR of D2H (Fig. 3). After the stimulating effect of FACE on P. nigra and P. × euramericana during the first year, second year-growth was larger in the control when expressed as a relative value. In the third year, RGR was once again higher (although slightly) in FACE than in the control for all species. RGR decreased considerably from the first to the third year. The relationship between tree AGR and D2H showed a significant species effect on slope but not on the intercept for the 3 yr (Table 3). A significant effect of treatment (P < 0.0001) was observed in the first year, with a steeper slope in the FACE treatment. On the contrary, the slope was smaller in the FACE treatment in the second year (P = 0.005), although the intercept was larger (P = 0.02) than in the control treatment. In the third year, no differences between treatments were observed (Table 3).

image

Figure 2. Effect of FACE treatment on stem volume index (D2H) for Populus alba (square), Populus nigra (triangle) and Populus × euramericana (circle) grown for 3 yr under control and FACE treatments. Symbols represent the ratio between mean values in FACE and control treatments.

Download figure to PowerPoint

image

Figure 3. Mean (averaged over each year) daily relative growth rate (RGR) of D2H (+ SE) calculated for the first, second, and third years in control (open bars) and FACE (closed bars) treatments for three Populus species. Each value represents the mean + SE of 3 plots.

Download figure to PowerPoint

Table 3.  Levels of significance (P-values) according to analysis of covariance (ANCOVA) between absolute growth rate of D2H (AGR) of individual poplar trees and their corresponding D2H (covariate) during a 4-wk period of the first part of each growing season
 D2HTreatSpeciesD2H × TreatD2H × Species
First year< 0.00010.530.24< 0.00010.0002
Second year< 0.00010.020.950.005< 0.0001
Third year< 0.00010.350.190.240.0002

Taper index calculated on 3-yr-old stems showed significant differences only among species (P = 0.02) but not between treatments (P = 0.27). Only in P. alba, values were quite different with 0.43 in control and 0.39 in FACE, whereas for P. nigra and P. × euramericana values ranged between 0.44 and 0.46, depending on the treatment.

Competition

The coefficient of variation of stem BA was always smaller in the FACE treatment (Fig. 4). Overall, the treatment effect was only significant at the end of the third year (P = 0.039), and not at the end of the first year (P = 0.083) or the second year (P = 0.141). Comparison of means for each species separately, did not show significant treatment effects. Species differences were significant in the second and third years. We observed a decrease of stand size variability between the end of the first and the second year, followed by an increase in the third year (Fig. 4).

image

Figure 4. Coefficients of variation for stem BA of three Populus species in control (open symbols) and FACE (closed symbols) treatments measured at the end of each year. Values are means ± SE of 3 plots.

Download figure to PowerPoint

Frequency distribution of single tree CI values was not different between treatments (P = 0.43) although for each competition class mean DBH values resulted higher in the FACE treatment (Table 4). The relationship between CI values and relative RGR of BA evidenced no species (P = 0.15 and 0.46 for intercept and slope, respectively) effect. Nevertheless a significant treatment effect (P = 0.06 and 0.03 for intercept and slope, respectively) was observed for RGR of BA and this was mainly evident for P. nigra and P. × euramericana (Fig. 5).

Table 4.  Frequency distribution of poplar trees grown under control and free-air CO2 enrichment (FACE) treatments for 3 yr categorized by competition class
Competition ClassNo. of treesMean DBH (mm)Mean CI
ControlFACEControlFACEControlFACE
  1. Data from the different species are merged. For each competition class the mean diameter at breast height (DBH) and the mean CI (competition index) value is calculated.

CI ≤ 6171659.061.2 5.20 5.65
6 < CI ≤ 8384348.553.5 6.80 6.78
8 < CI ≤ 10 9 737.443.3 8.96 8.58
CI > 10 6 327.430.812.0011.90
image

Figure 5. Relationship between competition index (CI) values and mean daily relative growth rate (RGR) of BA for trees of Populus alba (square), Populus nigra (triangle) and Populus × euramericana (circle) under control (open symbols and dashed line) and FACE (closed symbols and continuous line) treatments on the third year of growth.

Download figure to PowerPoint

Branches

Data on the production of sylleptic branches confirmed species-specific differences (Tables 2 and 5). In all years, P. × euramericana was characterized by a very strong apical dominance and a small production of sylleptic branches concentrated in the first part of the growing season. P. alba produced a moderate amount of sylleptic branches throughout each growing season, whereas P. nigra produced a large number of sylleptic branches during the first half of each growing season.

Table 5.  Mean values (± SE) of branches produced per tree in three Populus species, grown for 3 yr under control and free-air CO2 enrichment (FACE) treatments
  P. albaP. nigraP. x euramericana
  1. syll, sylleptic branches; prol, proleptic branches; HGI, height growth increment; RSBPR, relative sylleptic branches production rate (No. d−1 m−1). Each value represents the mean value of 3 plots.

No. syll HGI 1control13.5 (3.6)33.8 (2.6) 3.9 (1.3)
FACE15.4 (2.6)46.3 (1.1) 9.6 (1.6)
RSBPR HGI 1control 0.081 (0.016) 0.216 (0.018) 0.038 (0.012)
FACE 0.087 (0.009) 0.247 (0.002) 0.084 (0.013)
No. syll HGI 2control56.5 (3.3)62.4 (5.7) 3.1 (2.3)
FACE52.6 (1.3)58.2 (7.0) 5.7 (1.4)
RSBPR HGI 2control 0.071 (0.003) 0.088 (0.006) 0.004 (0.003)
FACE 0.059 (0.003) 0.084 (0.010) 0.008 (0.003)
No. prol HGI 1control38.3 (0.4)38.9 (3.7)29.3 (5.4)
FACE38.7 (0.5)31.8 (1.5)28.3 (3.5)
No. prol HGI 1 m−1control27.9 (2.4)23.2 (2.2)22.6 (1.3)
FACE25.0 (2.2)17.4 (0.7)18.3 (2.3)
No. syll HGI 3control29.1 (2.9)41.5 (7.9)14.2 (1.0)
FACE29.1 (4.0)45.6 (2.0)11.0 (1.1)
RSBPR HGI 3control 0.051 (0.002) 0.080 (0.014) 0.036 (0.003)
FACE 0.048 (0.005) 0.079 (0.003) 0.025 (0.003)
No. prol HGI 2control20.4 (0.9)41.8 (3.8)63.6 (2.0)
FACE24.2 (1.4)45.7 (6.6)58.6 (0.4)
No. prol HGI 2 m−1control 4.8 (0.4)10.0 (1.0)14.4 (0.6)
FACE 5.2 (0.2)10.8 (1.5)13.7 (0.7)

Sylleptic branch production was stimulated by the FACE treatment in the first year (Table 2) in P. nigra (P = 0.01) and in P. × euramericana (although not significantly for this species). Part of this effect originated from size differences, in particular from the main stem length. This was overcome by using the RSBPR, which was only slightly, but not significantly, different between treatments, although differences among species remained very prominent.

In the second year, the RSBPR decreased for all species, in particular for P. nigra and P. × euramericana. The number of sylleptic branches produced per tree in the second year was higher than in the first for P. alba and P. nigra, partly due to the longer growing season and to the larger tree dimensions. Only for P. × euramericana, sylleptic branch production per tree was higher in the FACE treatment. In the third year, differences between treatments in the number of sylleptic branches and in RSBPR were small for all species. Branch production of P. × euramericana increased considerably compared to the first 2 yr, especially in the control treatment (Table 5).

All proleptic branches originated at the beginning of the growing seasons (second and third); some of them died and fell during the season of origin. Small differences in the number of proleptics were observed between treatments and among species in the second year and values per unit of stem HGI were higher in the control for all species. On the contrary, clear differences among species were observed in the third year: P. × euramericana produced considerably more proleptic branches than P. nigra and three times as many as P. alba (Table 5).

A significant treatment effect was observed at the end of the first year on sylleptic branches BA (Table 2). This was significant for P. nigra (P < 0.001), but not for P. × euramericana or for P. alba, where a small stimulating effect was observed. These differences persisted at the end of the second year for sylleptic branches produced during the first year. No treatment effect was observed for the BA of proleptic or sylleptic branches produced during the second year. The most productive species in terms of branch BA was P. nigra (Fig. 6). A very strong effect of species (P < 0.0001) was observed in all analyses of sylleptic branching, whereas much less difference was apparent in proleptic branching. It should be highlighted that after 2 yr, despite different absolute values between control and FACE, the ratio of stem BA to branch BA remained constant in both treatments for all species: 0.525 for P. alba, 0.62 for P. nigra and 1.255 for P. × euramericana (Fig. 6), as average of the two treatments. Further information on branch properties is contained in Gielen et al. (2002).

image

Figure 6. Distribution of basal area over stem and branches at the end of the second year under control (C) and FACE (F) treatments for three Populus species. Each value represents the mean + SE (of total value) of 3 plots. The ratio of stem BA to branch BA is indicated within the bars for each species and treatment. HGI X, height growth increment of year X.

Download figure to PowerPoint

Bud phenology

There was a very small effect of FACE on the dates of bud burst and bud set in all years. The only differences observed between treatments were a delay in bud set of 7 d in FACE for P. nigra in the first year and a delay of 5 d in the control for P. × euramericana in the second year (Table 6). It was very unlikely that this influenced overall growth. Bud burst in the second and in the third years differed only slightly among species, with up to 1 wk of difference in the occurrence of bud burst phases.

Table 6.  Dates of bud set and bud burst (± se) of apical buds for three Populus species grown for 3 yr under control and free-air CO2 enrichment (FACE) treatments and subsequent calculation of the length of the growing seasons
  P. alba P. nigraP. × euramericana
  1. Date of bud burst corresponds to class 4 on the phenology scale (see Material and Methods). Each value represents the mean value of 3 plots. *, the beginning of the first growing season was set as 1 July.

1st year
Bud setcontrolOct, 25 (0.6)Oct, 03 (1.0)Sep, 10 (0.2)
FACEOct, 26 (0.3)Oct, 10 (0.8)Sep, 10 (0.1)
Growing season (days)*control116 94 71
FACE117101 71
2nd year
Bud burstcontrolApr, 13 (1.5)Apr, 07 (1.0)Apr, 07 (1.5)
FACEApr, 13 (1.5)Apr, 10 (0.0)Apr, 07 (1.5)
Bud setcontrolOct, 22 (1.8)Sep, 22 (0.6)Sep, 05 (0.4)
FACEOct, 22 (1.7)Sep, 21 (0.2)Aug, 31 (1.0)
Growing season (days)control192168151
FACE192164146
3rd year
Bud burstcontrolApr, 04 (0.0)Apr, 02 (1.7)Apr, 03 (0.7)
FACEApr, 04 (0.0)Apr, 02 (0.0)Apr, 02 (0.7)
Bud setcontrolOct, 15 (1.6)Sep, 24 (1.1)Sep, 01 (0.8)
FACEOct, 14 (1.6)Sep, 24 (1.4)Sep, 02 (1.3)
Growing season (days)control195175151
FACE194175153

On the contrary, strong differences among species were observed on dates of bud set. P. alba was characterized by the longest growing season, which lasted until the middle or the end of October depending on the year. P. nigra set the apical bud around the end of September and the beginning of October whereas P. × euramericana 20–30 d earlier. Due to differences in bud set, the growing season of P. alba was on average 25 d longer than P. nigra and 40 d longer than P. × euramericana. This allowed a recovery by P. alba of the height differences registered in the middle of each growing season.

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Although the first evident result is a significant FACE effect on growth parameters after 3 yr of exposure – also confirmed by biomass data (Calfapietra et al., 2003) – this paper aims to analyse the dynamics of growth in each of the 3 yr characterized by extremely different conditions of the stand. The response to elevated CO2 differed between the first and the second year, whereas fewer differences were evidenced between the second and the third year. The maximum LAI reached values between 4 and 5 in the second year (Gielen et al., 2001) and between 5 and 8 in the third year, depending on the species and treatment (Gielen et al., 2003), providing evidence of canopy closure and the onset of strong competition amongst trees. Growth stimulation by the FACE treatment started immediately after planting for P. nigra and P. × euramericana as demonstrated by the dynamics of BA and height (Fig. 1a,b) and the CO2 effect on D2H (Fig. 2). This initial stimulation during the first phase of CO2 treatment is in line with that demonstrated for various herbaceous and tree species (Bazzaz et al., 1993; Poorter et al., 1996) as well as for clones of cherry and Sitka spruce (Centritto et al., 1999).

The POPFACE experiment clearly demonstrated species-specific differences in the extent of CO2 stimulation. The response was weak for P. alba and only became evident 2 months after planting, whereas it was particularly rapid and strong for P. nigra, resulting in a doubling of the D2H in FACE when compared with the control treatment at the end of the first year. The positive response was caused by an increase in BA rather than in height, which was stimulated by about 10% in the FACE treatment for all species (Table 1). Nevertheless the treatment effect on height was significant at the end of the first and the third years (Table 2). Similar observations were made by Tognetti et al. (1999) on poplar and by Percy et al. (2002) on aspen.

During the second year, stimulation under elevated CO2 was lost and RGR of D2H became higher in ambient CO2 (Fig. 3). However, at the end of the second year the size of FACE trees, namely BA and D2H, remained significantly bigger than control trees.

It should be emphasized that comparing growth in the control and FACE treatments was complicated at the onset of the second growing season because of treatment related size differences. Many studies have shown that elevated CO2 causes an enhancement of plant development, especially during the early stages (Bazzaz et al., 1993; Norby et al., 1995), but later growth can be very similar when analysing plants of similar size rather than at the same time (Centritto et al., 1999), as was observed in our experiment. When comparing the AGR in control and FACE treatments at similar tree sizes the stimulating effect of FACE was very prominent in the first year but not in the others, which was supported by our analysis of covariance (Table 3). In the second year, slope was higher in control but intercept was higher in FACE, which suggests that overall growth was not different between treatments. We hypothesize that higher values of second-year RGR of D2H in the control treatment are simply due to the larger size of trees in the FACE treatment, which had ontogenetically reduced the response of plants to elevated CO2 (Jarvis & Jarvis, 1964; Evans, 1972). This is confirmed by negative correlations between RGR of BA and BA in the second year. The reduction in growth rate has also been explained as a reduction of assimilation referred to as acclimation (Brown, 1991; Ceulemans & Mousseau, 1994). However, this explanation does not fit our observations since the ratio between AGR and corresponding values of leaf area during the second year was similar between both treatments, or even higher in FACE (data not shown). Since leaf area is one of the main factors determining tree productivity, it is possible to conclude that there was no reduction of growth in FACE compared to the control treatment in the second year. Moreover, no physiological acclimation emerged from leaf gas exchange measurements (Bernacchi et al., 2003).

With regard to this issue, we investigated whether the FACE-induced first-year's stimulation could have affected competition in these high-density stands. The coefficient of variation in this study decreased from the first to the second year, and increased again in the third year, which is usually explained by two-sided competition during the second year, and the onset of asymmetric competition in the third year (Weiner, 1985; Weiner & Thomas, 1986). This was confirmed by our observations of RGR of BA vs BA; small trees exhibit larger RGR as compared to large trees in the absence of asymmetric competition, and RGR is similar among tree size classes in an early stage of competition (Ford, 1976; Perry, 1985; Soares & Tomé, 1996). Our results are similar to those of eucalypt plantations that evolved from two-sided to asymmetric competition near the time of canopy closure (Toméet al., 1994; Soares & Tomé, 1996). Therefore, competition was probably mainly for nutrients and/or water in the second year, and was more asymmetric in the third year when light became limiting (Weiner, 1986; Soares & Tomé, 1996). Coefficients of size variation were observed to be lower in FACE; however, these observations may be caused by initial differences in variation.

In the third year we did not observe a significant variation of individual CI values between treatments, although the relationship between individual CI values and corresponding RGR of BA was significantly affected by the FACE treatment. Trees grown under elevated CO2 showed an increased RGR at the lowest competition levels and a decreased RGR at the highest competition levels compared to the control (Fig. 5). This cannot be explained by the mean bigger size of the FACE trees (Table 4) because this was evident for all the competition classes, and moreover RGR of BA had a positive correlation with size in the third year. Our finding agrees with McDonald et al. (2002) who observed the greater positive response to elevated CO2 for competitively advantaged trees.

The biomass present on branches should not be neglected since it made up a relevant part of the total production in particular for P. alba and P. nigra. The stimulation of sylleptic branch production during the first year was one of the most evident effects of the FACE treatment, except for P. alba. Increased branch production in elevated CO2 was also observed by Idso et al. (1991), Norby et al. (1996) and on poplars by Ceulemans et al. (1995) and Tognetti et al. (1999). This seems to represent a way for the plant to invest surplus carbohydrates derived from the increased photosynthetic rate and/or leaf area, which usually occurs under elevated CO2. The first year-stimulation of sylleptic branch production was confirmed by increased LAI values (Gielen et al., 2001), particularly for P. nigra. Increased LAI was due to an increased number of branches but also to increased leaf size in the FACE treatment (Ferris et al., 2001; Gielen et al., 2001). The number of sylleptic branches per tree could have been influenced by the larger size of trees in elevated CO2, although the length of the stem differed only slightly between treatments. Values of RSBPR confirmed the differences between treatments, even taking into account the differences in the length of the growing season (Tables 5 and 6). Stimulation of sylleptic branch production by FACE was lost in the second year in line with observations of other growth parameters.

The number of proleptic branches produced in the second year per unit of stem length was higher in control than in FACE, possibly because the larger space not occupied by sylleptic branches increased bud availability for generating proleptic branches. The number of proleptic branches produced during the second year was very similar for all species, unlike the number of proleptic branches produced in the third year. Most of them developed very quickly at the beginning of each growing season and died after a few months, even at canopy levels with high light levels. At the end of the second year, the component of BA represented by proleptic branches was particularly large in P. × euramericana, whereas it was relatively small in P. nigra and P. alba, which invested mainly in sylleptic branches (Fig. 6).

After 2 yr the BA of stem and of total branches were shown to be highly correlated with a constant ratio typical for each species (Fig. 6).

Dates of bud burst did not differ significantly among species or between treatments. Bud set, however, differed by almost 50 d between P. × euramericana and P. alba, although the longer growing season was not sufficient for P. alba to catch-up with the stem growth of the two other species. FACE treatment did not significantly influence date of bud set in any year; there were small differences for P. nigra in the first year and for P. × euramericana in the second. This finding disagreed with previous reports of a clear effect of elevated CO2 on bud phenology. For example Ceulemans et al. (1995) observed delayed bud burst in elevated CO2 for one genotype of Populus grown in open top chambers, whereas another genotype exhibited advanced bud set. The same behaviour was observed by Sigurdsson (2001) on P. trichocarpa. Picea sitchensis and Castanea sativa growing in pots in field chambers exhibited both delayed bud burst and advanced bud set (El Kohen et al., 1993; Murray et al., 1994). However, in different experiments on trees no effect of elevated CO2 on bud phenology was found (Johnsen & Seiler, 1996; Rey & Jarvis, 1997; Murray & Ceulemans, 1998).

In conclusion, size of three poplar species was significantly enhanced under CO2 enrichment in POPFACE after 3 yr of exposure. The stimulation was strong in the first year but did not occur in the second and third year. This result was confirmed by comparing tree growth in different treatments at the same size. Expected differences among species were observed in both treatments. Moreover during the third year, characterized by the presence of strong competition (asymmetric competition), growth resulted stimulated under FACE treatments for competitively advantaged trees but not for disadvantaged ones.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

This research was conducted under the following programmes: EU-POPFACE (ENV4-CT97-0657), Center of Excellence ‘Forest and Climate’ (MIUR Italian Ministry of University and Research), MIUR-COFIN 2000 (coord. Marco Borghetti). The authors acknowledge P. Tricker (University of Southampton) for language revision, T. Crowe (University of Southampton) and S. Van Dongen (University of Antwerpen) for statistical advise. We also thank T. Oro, P. Pinacoli and M. Tamantini for technical assistance, as well as G. Cortignani, I. Janssens, A. Claus, M. Lukac, G. Avino, B. Bartoli and V. De Sousa for their help during the field campaigns. B. Gielen is a Research Assistant of the Fund for Scientific Research-Flanders (F.W.O.-Vlaanderen).

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • Bazzaz FA, Miao SL, Wayne PM. 1993. CO2-induced growth enhancements of co-occurring tree species decline at different rates. Oecologia 96: 478482.
  • Beaton A, Thompson D, Webber J. 1991. British poplar-a 21st century challenge. Forestry and British Timber August: 1921.
  • Bernacchi CJ, Calfapietra C, Davey PA, Wittig VE, Scarascia-Mugnozza GE, Raines CA, Long SP. 2003. Photosynthesis and stomatal conductance responses of poplars to free-air CO2 enrichment (PopFACE) during the first growth cycle and immediately following coppice. New Phytologist 159: 609621.
  • Bosac C, Gardner SDL, Taylor G, Wilkins D. 1995. Elevated CO2 and hybrid poplar: a detailed investigation of root and shoot growth and physiology of P. euramericana‘Primo’. Forest Ecology and Management 74: 103116.
  • Brown KR. 1991. Carbon dioxide enrichment accelerates the decline in nutrient status and relative growth rate of Populus tremuloides Michx. seedlings. Tree Physiology 8: 161173.
  • Calfapietra C, Gielen B, Galema ANJ, Lukac M, De Angelis P, Moscatelli MC, Ceulemans R, Scarascia-Mugnozza G. 2003. Free-air CO2 enrichment (FACE) enhances biomass production in a short-rotation poplar plantation (POPFACE). Tree Physiology 23: 805814.
  • Calfapietra C, Gielen B, Sabatti M, De Angelis P, Scarascia-Mugnozza G, Ceulemans R. 2001. Growth performance of Populus exposed to ‘Free Air Carbon dioxide Enrichment’ during the first growing season in the POPFACE experiment. Annals of Forest Science 58: 819828.
  • Castellani E, Freccero V, Lapietra GF. 1967. Proposta di una scala di differenziazione delle gemme fogliari del pioppo utile per gli interventi antiparassitari. Giornale Botanico Italiano 101: 355360.
  • Centritto M, Lee HSJ, Jarvis PG. 1999. Increased growth in elevated (CO2): an early, short-term response? Global Change Biology 5: 623633.
  • Ceulemans R, Deraedt W. 1999. Production physiology and growth potential of poplars under short-rotation forestry culture. Forest Ecology and Management 121: 923.
  • Ceulemans R, Impens I, Mau F, Van Hecke P, Chen SG. 1992. Dry mass production and solar radiation conversion efficiency of poplar clones. In: GrassiG, CollinaA, ZibettaH, eds. Biomass for Energy, Industry and Environment: 6th E.C. Conference. London, UK: Elsevier, 157163.
  • Ceulemans R, Jiang XN, Shao BY. 1995. Effects of elevated atmospheric CO2 on growth, biomass production and nitrogen allocation of two Populus clones. Journal of Biogeography 22: 261268.
  • Ceulemans R, Mousseau M. 1994. Tansley Review, 71. Effects of elevated atmospheric CO2 on woody plants. New Phytologist 127: 425446.
  • Curtis PS, Vogel CS, Pregitzer KS, Zak DR, Teeri JA. 1995. Interacting effects of soil fertility and atmospheric CO2 on leaf area-growth and carbon gain physiology in Populus×euramericana (Dode) Guinier. New Phytologist 129: 253263.
  • DeLucia EH, Hamilton JG, Naidu SL, Thomas RB, Andrews JA, Finzi A, Lavine M, Matamala R, Mohan JE, Hendrey GR, Schlesinger WH. 1999. Net primary production of a forest ecosystem with experimental CO2 enrichment. Science 284: 11771179.
  • Dickson RE, Lewin KF, Isebrands JG, Coleman MD, Heilman WE, Riemenschneider DE, Sober J, Host GE, Hendrey GR, Pregitzer KS, Karnosky DF. 2000. Forest atmosphere carbon transfer and storage (FACTS II) – The Aspen free-air CO2 and O3 enrichment (FACE) project: An overview. USDA Forest Service, North Central Forest Experiment Station. General Technical Report NC-214.
  • Dixon RK, Brown S, Houghton RA, Solomon AM, Trexler MC, Wisniewski J. 1994. Carbon pools and flux of global forest ecosystems. Science 263: 185189.
  • Eamus D, Jarvis PG. 1989. The direct effects of increase in the global atmospheric CO2 concentration on natural and commercial temperate trees and forests. Advances in Ecological Research 19: 255.
  • El Kohen A, Venet L, Mousseau M. 1993. Growth and photosynthesis of two deciduous forest tree species exposed to elevated carbon dioxide. Functional Ecology 7: 480486.
  • Evans GC. 1972. Relative growth rate. In: AndersonDJ, Greigh-SmithP, PitelkaFA, eds. The quantitative analysis of plant growth. Oxford, UK: Blackwell Scientific Publications, 246254.
  • Ferris R, Sabatti M, Miglietta F, Mills R, Taylor G. 2001. Leaf area is stimulated in Populus by free-air CO2 enrichment (POPFACE), through increased cell expansion and production. Plant, Cell & Environment 24: 305316.
  • Ford ED. 1976. Competition, genetic systems and improvement of forest yield. In: CannellMGR, LastFT, eds. Tree physiology and yield improvement. London, UK: Academic Press, 463472.
  • Friend AL, Scarascia-Mugnozza G, Isebrands J, Heilman PE. 1991. Quantification of two-year-old hybrid poplar root systems: morphology, biomass, and 14C distribution. Tree Physiology 8: 109119.
  • Galinski W, Goosens R, Ceulemans R, Impens I. 1991. The wood productivity of two poplar clones (Populus trichocarpa × Populus deltoides) as affected by stocking and age. Biomass Bioenergy 1: 233239.
  • Gardner SDL, Taylor G, Bosac C. 1995. Leaf growth of hybrid poplar following exposure to elevated CO2. New Phytologist 131: 8190.
  • Gielen B, Calfapietra C, Claus A, Sabatti M, Ceulemans R. 2002. Crown architecture of Populus spp. is differentially modified by free-air CO2 enrichment (POPFACE). New Phytologist 153: 91100.
  • Gielen B, Calfapietra C, Sabatti M, Ceulemans R. 2001. Leaf area dynamics in a closed poplar plantation under free-air carbon dioxide enrichment. Tree Physiology 21: 12451255.
  • Gielen B, Liberloo M, Bogaert J, Calfapietra C, De Angelis P, Miglietta F, Scaracia-Mugnozza G, Ceulemans R. 2003. Three years of free-air CO2 enrichment (POPFACE) only slightly affect profiles of light and leaf characteristics in closed canopies of Populus. Global Change Biology 9: 10221037.
  • Hansen EA. 1991. Poplar woody biomass yields: a look to the future. Biomass and Bioenergy 1: 17.
  • Hegyi F. 1974. A simulation model for managing jack-pine stands. In: FriesJ, ed. Growth models for tree and stand simulation. Stockholm, Sweden: Royal College of Forestry. 7490.
  • Hendrey GR, Lewin KF, Nagy J. 1993. Free-air carbon dioxide enrichment: development, progress, results. Vegetatio 104/105: 1731.
  • Holmes MJ, Reed DD. 1991. Competition indexes for mixed species northern hardwoods. Forest Science 37: 13381349.
  • Hunt R. 1982. Plant growth curves: the functional approach to plant growth analysis. London, UK: Edward Arnold.
  • Idso SB, Kimball BA, Allen SG. 1991. CO2 enrichment of sour orange trees: 2.5 years into a long-term experiment. Plant, Cell & Environment 14: 351353.
  • Isebrands JG, McDonald EP, Kruger E, Hendrey G, Pregitzer K, Percy K, Sober J, Karnosky DF. 2001. Growth responses of Populus tremuloides clones to interacting carbon dioxide and tropospheric ozone. Environmental Pollution 115: 359371.
  • Jarvis PG. 1998. European Forests and Global Change: the Likely Impacts of Rising CO2 and Temperature. Cambridge, UK: Cambridge University Press.
  • Jarvis PG, Jarvis MS. 1964. Growth rates of woody plants. Physiologia Plantarum 17: 654666.
  • Johnsen KH, Seiler JR. 1996. Growth, shoot phenology and physiology of diverse seed sources of black spruce. I. Seedling responses to varied atmospheric CO2 concentrations and photoperiods. Tree Physiology 16: 367373.
  • Kalina J, Ceulemans R. 1997. Clonal differences in the response of dark and light reactions of photosynthesis to elevated atmospheric CO2 in poplar. Photosynthetica 33: 5161.
  • King JS, Pregitzer KS, Zak DR, Sober J, Isebrands JG, Dickson RE, Hendrey GR, Karnosky DF. 2001. Fine root biomass and fluxes of soil carbon in young stands of paper birch and trembling aspen as affected by elevated atmospheric CO2 and tropospheric O3. Oecologia 128: 237250.
  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD. 1996. SAS system for mixed models. Cary, NC, USA: SAS Institute Inc.
  • MacPherson G. 1995. Home-grown energy from short-rotation coppice. Ipswich, UK: Farming Press Books.
  • Madgwick HAI. 1971. The accuracy and precision of estimates of the dry matter in stems, branches, and foliage in an old-field Pinus virginiana stand. In: YoungHE, ed. Forest Biomass Studies. Orono, ME, US: University Main Press, 105–112.
  • McDonald EP, Kruger EL, Riemenschneider DE, Isebrands JG. 2002. Competitive status influences tree-growth responses to elevated CO2 and O3 in aggrading aspen stands. Functional Ecology 16: 792801.
  • Miglietta F, Peressotti A, Vaccari FP, Zaldei A, De Angelis P, Scarascia-Mugnozza G. 2001. Free-air CO2 enrichment (FACE) of a poplar plantation: the POPFACE fumigation system. New Phytologist 150: 465476.
  • Murray MB, Ceulemans R. 1998. Will tree foliage be larger and live longer? In: JarvisPG, ed. European forests and global change: likely impacts of rising CO2 and temperature. Cambridge, UK: Cambridge University Press, 94125.
  • Murray MB, Smith RI, Leith ID, Fowler D, Lee HSJ, Friend AD, Jarvis PG. 1994. Effects of elevated CO2, nutrition and climatic warming on bud phenology in Sitka spruce (Picea sitchensis) and their impact on the risk of frost damage. Tree Physiology 14: 691706.
  • Norby RJ, Todd DE, Fults J, Johnson DW. 2001. Allometric determination of tree growth in a CO2-enriched sweetgum stand. New Phytologist 150: 477487.
  • Norby RJ, Wullschleger SD, Gunderson CA. 1996. Tree responses to elevated CO2 and the implications for forests. In: KochGW, MooneyHA, eds. Carbon dioxide and terrestrial ecosystem. San Diego, CA, USA: Academic Press, 121.
  • Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R. 1999. Tree responses to rising CO2 in field experiments: implications for the future forest. Plant, Cell & Environment 22: 683714.
  • Norby RJ, Wullschleger SD, Gunderson CA, Nietch CT. 1995. Increased growth efficiency of Quercus alba trees in a CO2-enriched atmosphere. New Phytologist 131: 9197.
  • Oechel WC, Strain BR. 1985. Native species responses to increased atmospheric carbon dioxide concentration. In: StrainBR, CureJD, eds. Direct effects of increasing carbon dioxide on vegetation. Department of Energy, Office of Basic Energy Sciences, Carbon Dioxide Research Division, Springfield, Washington DC, USA, 117154.
  • Percy KE, Awmack CS, Lindroth RL, Kubiske ME, Kopper BJ, Isebrands JG, Pregitzer KS, Hendrey GR, Dickson RE, Zak DR, Oksanen E, Sober J, Harrington R, Karnosky DF. 2002. Altered performance of forest pests under CO2- and O3-enriched atmospheres. Nature 420: 403407.
  • Perry DA. 1985. The competition process in forest stands. In: CannellMGR, JacksonJE, eds. Trees as crop plants. Natural Environment Research Council, UK: Institute of Terrestrial Ecology, 481506.
  • Piutti E, Cescatti A. 1997. A quantitative analysis of the interactions between climatic response and intraspecific competition in European beech. Canadian Journal of Forest Research 27: 277284.
  • Pontailler JY, Ceulemans R, Guittet J, Mau F. 1997. Linear and non-linear functions of Volume index to estimate woody biomass in high density young poplar stands. Annual Science of Forestry 54: 335345.
  • Poorter H. 1993. Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. Vegetatio 104/105: 7797.
  • Poorter H, Roumet C, Campbell BD. 1996. Interspecific variation in the growth response of plants to elevated CO2: a search for functional types. In: KörnerC, BazzazFA, eds. Carbon dioxide, populations, and communities. London, UK: Academic Press Inc., 375412.
  • Pregitzer KS, Zak DR, Curtis PS, Kubiske ME, Teeri JA, Vogel CS. 1995. Atmospheric CO2, soil nitrogen and turnover of fine roots. New Phytologist 129: 579585.
  • Radoglou KM, Jarvis PG. 1990. Effects of CO2 enrichment on four poplar clones. I. Growth and leaf anatomy. Annals of Botany 65: 617626.
  • Remphrey WR, Powell GR. 1985. Crown architecture of Larix laricina saplings: sylleptic branching on the main stem. Canadian Journal of Botany 63: 12961302.
  • Rey A, Jarvis PG. 1997. Growth response of young birch trees (Betula pendula Roth.). In: MohrenGMJ, KramerK, SabatéS, eds. Impacts of global change on tree physiology and forest ecosystems. Dordrecht, The Netherlands: Kluwer Academic Publishers, 207212.
  • Saxe H, Ellsworth DS, Heath J. 1998. Tree and forest functioning in an enriched CO2 atmosphere. New Phytologist 139: 395436.
  • Scarascia-Mugnozza GE, Ceulemans R, Heilman PE, Isebrands JG, Stettler RF, Hinckley TM. 1997. Production physiology and morphology of Populus species and their hybrids grown under short rotation. II. Biomass components and harvest index of hybrid and parental species clones. Canadian Journal of Forest Research 27: 285294.
  • Scarascia-Mugnozza G, De Angelis P, Sabatti M, Calfapietra C, Ceulemans R, Peressotti A, Miglietta F. 2000. A FACE experiment on short rotation, intensive poplar plantation: objective and experimental set up of POPFACE. In: SuttonMA, MorenoJM, Van Der PuttenWH, StruweS, eds. Terrestrial ecosystem research in europe: successes, challenges and policy. Luxembourg: Office for Official Publications of the European Communities, 136140.
  • Schimel D, Alves D, Enting D, Heimann M, Joos F. 1996. Radiative forcing of climate change. In: HoughtonJT, FilhoLGM, CallanderBA, HarrisN, KattenbergA, MaskellK, eds. Climate change 1995: the science of climate change. Cambridge, UK: Cambridge University Press, 65132.
  • Sigurdsson BD. 2001. Elevated (CO2) and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a three-year field study. Trees 15: 403413.
  • Soares P, Tomé M. 1996. Changes in eucalypt plantations structure, variability and relative growth rate pattern under different intraspecific competition gradients. In: SkovsgaardJP, JohannsenVK, eds. Modelling Regeneration Success and Early Growth of Forest Stands, Proceedings from the IUFRO Conference. Copenhagen, Denmark: Danish Forest and Landscape Research Institute, 270284.
  • Tognetti R, Longobucco A, Raschi A, Miglietta F, Fumagalli I. 1999. Responses of two Populus clones to elevated atmospheric CO2 concentration in the field. Annals of Forest Science 56: 493500.
  • Tomé M, Burkhart HE. 1989. Distance-dependent competition measures for predicting growth of individual trees. Forest Science 35: 816831.
  • Tomé M, Tomé JA, Araújo MC, Pereira JS. 1994. Intraspecific competition in irrigated and fertilized eucalypt plantations. Forest Ecology and Management 69: 211218.
  • Verwijst T. 1991. Logarithmic transformations in biomass estimation procedures: violation of the linearity assumption in regression analysis. Biomass and Bioenergy 1: 175180.
  • Weiner J. 1985. Size hierarchies in experimental populations of annual plants. Ecology 66: 743752.
  • Weiner J. 1986. How competition for light and nutrients affects size variability in Ipomoea tricolor populations. Ecology 67: 14251427.
  • Weiner J, Thomas CS. 1986. Size variability and competition in plant monocultures. Oikos 47: 211222.