Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:
Tree Physiology 16, 61--68
© 1996 Heron Publishing----Victoria, Canada
First- and second-year aboveground growth and productivity of two
Populus hybrids grown at ambient and elevated CO2
R. CEULEMANS,1 B. Y. SHAO,1 X. N. JIANG2 and J. KALINA3
1
Department of Biology, University of Antwerpen (UIA), Universiteitsplein 1, B-2610 Wilrijk, Belgium
2
Experimental Center of Forest Biology, Beijing Forestry University, 100083 Beijing, Peoples Republi
c of China
3
Academy of Sciences of the Czech Republic, Institute of Landscape Ecology, Department of Ecological
Physiology of Forest Trees, CS-60300 Brno,
Czech Republic
Received March 2, 1995
Summary Two hybrid poplar (Populus) clones (the fastgrowing clone Beaupré (P. trichocarpa Torr. and Gray × P. deltoides Bartr. ex Marsh.) and the slow-growing clone Robusta
(P. deltoides Bartr. ex Marsh. × P. nigra L.)) were grown from
hardwood cuttings for one or two growing seasons (1993-1994) in either ambient or elevated (= ambient + 350 µmol
mol −1) CO2 in open-top chambers at the University of Antwerpen. Both clones responded positively to the elevated CO2
treatment with increased stem volume and aboveground
biomass production; however, the clones exhibited different
response strategies to the elevated CO2 treatment, and the
responses varied with cutting age and duration of exposure.
Clone Beaupré responded to the elevated CO2 treatment with
increases in leaf area and leaf area index during both the first
and second growing seasons, but little increase in height
growth. Clone Robusta exhibited increased height growth, leaf
biomass and total leaf nitrogen content in response to elevated
CO2, but no increase in leaf area index. The elevated CO2
treatment increased the total number of branches and total
branch biomass in both clones during both growing seasons.
At the end of the first growing season, woody stem biomass of
the fast- and slow-growing clones was increased by 38 and
55%, respectively. At the end of the second growing season,
stem volume was increased by 43% in clone Beaupré and by
58% in clone Robusta. The increase in stem volume was a result
of the stimulation of both height and diameter growth in the
slow-growing clone, whereas only height growth was stimulated in the fast-growing clone. In the fall of the first growing
season, the average date of bud set in clone Robusta was
advanced by 4 days in the elevated CO2 treatment; there were
no other significant effects of the elevated CO2 treatment on
bud set. The elevated CO2 treatment enhanced leaf C/N ratios
in both clones in both years.
Keywords: branches, leaf area index, nitrogen content, poplar,
volume index.
Introduction
The growth of deciduous trees often increases by about 30% in
response to elevated concentrations of atmospheric CO2,
whereas the overall mean effect of elevated CO2 on total
aboveground biomass production (or total gross photosynthesis) ranges from 0.5 to 15% (Strain 1987, Norby 1989, Eamus
and Jarvis 1989, Mousseau and Saugier 1992, Ceulemans and
Mousseau 1994). However, among different tree genera as
well as among different species and genotypes within the same
genus, responses to elevated CO2 vary greatly (Norby et al.
1986, O’Neill et al. 1987, Radoglou and Jarvis 1990, Rogers
et al. 1994, Ceulemans and Mousseau 1994). For example, El
Kohen et al. (1993) observed that elevated CO2 had no effect
on leaf area of sweet chestnut, whereas it increased total leaf
area of beech plants. Duff et al. (1994) found significant
differences in the growth rates of two closely related eucalypt
species of northern Australia in response to CO2 enrichment.
Because tree responses to increasing atmospheric CO2 concentrations appear to be species- and genotype-specific, there
is an urgent need to obtain more detailed information on the
likely consequences of the predicted global CO2 change on
growth, development and productivity of forest trees. Accordingly, the ECOCRAFT research network, consisting of more
than 12 European university laboratories and research institutes, was established in 1990 with the overall objective of
examining the impacts of increasing atmospheric CO2 concentration and temperature on European forests. Within the framework of this network, we have studied the effects of elevated
atmospheric CO2 concentrations on the growth, physiology
and development of two genotypes of poplar (Populus). Poplar
species and hybrids were used because they are planted as high
productivity, short-rotation tree crops (e.g., Ceulemans et al.
1987, 1993) and generally show a large positive response to
short-term CO2 enrichment (Gaudillère and Mousseau 1989,
Radoglou and Jarvis 1990, Brown 1991) under controlled
environment conditions.
To examine the long-term effects of an increase in atmospheric CO2 concentration on two Populus clones, Beaupré
62
CEULEMANS, SHAO, JIANG AND KALINA
(P. trichocarpa Torr. and Gray × P. deltoides Bartr. ex Marsh.)
and Robusta (P. deltoides Bartr. ex Marsh. × P. nigra L.),
differing in growth performance, we exposed clonal cuttings to
elevated atmospheric CO2 concentrations for two growing
seasons in open-top chambers. Clone Beaupré is a fast-growing clone (Ceulemans et al. 1987, Radoglou and Jarvis 1990,
Barigah et al. 1994) and clone Robusta is a slow-growing clone
(Radoglou and Jarvis 1990, Barigah et al. 1994). The clones
exhibited different responses to elevated CO2 treatment, which
varied with cutting age and duration of exposure.
al. 1993), and then the individual leaf areas were summed to
obtain the total leaf area per plant. In the second year, only
dimensions of individual leaves on the current terminal leader
were measured, and branch dimensions and allometric relationships of branch diameter versus leaf area (Ceulemans et al.
1993) were used to determine total leaf area per plant. Leaf
area indices of each clone and each treatment were obtained by
dividing the total leaf area of 15 plants (first year) or eight
plants (second year) by the ground area (7 m2) of each OTC,
assuming no interclonal competition within each OTC.
Phenological observations
Materials and methods
Plant materials and planting pattern
Two hybrid poplar clones, the fast-growing interamerican
clone Beaupré and the slow-growing euramerican clone
Robusta, were raised from clonal hardwood cuttings (25 cm
long) in four open-top chambers (OTCs) at the University of
Antwerpen, Belgium. On April 22, 1993, the cuttings, 15 per
OTC (i.e., 7 to 8 plants of each clone), were planted in a circle
at a spacing of 0.6 m. The distance between adjacent OTCs
ranged from 8 to 10 m, and to reduce the boundary effect, each
OTC was surrounded by 19 plants. Before planting, the heavy
clay soil was excavated from each OTC to a depth of 50 cm and
replaced with fertile, black horticultural soil. Each OTC was
manually weeded, and all plants were automatically drip irrigated throughout the two growing seasons. Because nutrient
conditions were near optimal at the start of the experiment,
fertilizer was only applied once during the first growing season
and three times during the second growing season.
Open-top chamber design
Each decagonal OTC (3 m in diameter and 6 m in height) was
made of 1-m wide Plexiglas sheets and had a usable ground
area of 7 m2. Incoming chamber air was supplied by large
ventilators (S and P, CBM 320-65, Spain) at a rate of about
6500 m3 h −1, i.e., about two air volume changes per minute. Air
distribution within the OTC was effected through a flexible
spiroid pipe attached to a perforated polythene annulus 1 m
above the ground. Two OTCs provided a control treatment at
ambient atmospheric CO2 (about 350 µmol mol −1), and the
other two OTCs provided an elevated CO2 treatment at ambient
+ 350 µmol mol −1 (about 700 µmol mol −1). Input of CO2 was
controlled by a gas mass flowmeter (Model 5851E, Brooks
Instruments, Rosemount, The Netherlands) and was supplied
24 h per day from April 1993 until early November 1993 and
from mid-March 1994 until early November 1994. No CO2
enrichment was supplied from November 1993 to March 17,
1994.
Nondestructive height and leaf area measurements
Total plant height was monitored throughout each growing
season until November. Leaf area index (LAI) was determined
nondestructively for each clone and each treatment. In the first
year, individual leaf area was estimated by means of allometric
relations between leaf dimensions and leaf area (Ceulemans et
From September onward, observations on bud set and leaf fall
were made per clone and per treatment. Dates of bud set were
determined for terminal shoots as well as for branches (second
year). For all phenological observations, mean values (± SE)
of all plants (15 and eight plants per clone and per treatment in
the first and second year, respectively) were calculated.
Stem volume determinations
At the end of the first growing season, stem diameters at the
top and bottom of each plant were measured (in two perpendicular directions) with a caliper. Stem volume index was
estimated for each plant as (π/3)H(R12 + R1R2 + R22), where R1
and R2 are the radii at the bottom and the top of the stem,
respectively, and H is total plant height. At the end of the
second year, stem diameters of all harvested plants were measured at 1-m intervals. For each 1-m stem segment, the volume
was calculated based on the formula for a truncated cone as
above, but where R1 and R2 are the radii at the base and the top
of each stem segment, respectively, and H is the length of the
segment. Total stem volume per plant was obtained by summing the volumes of all individual stem segments (Causton
1985).
Destructive biomass measurements
At the end of November 1993, half of the plants (i.e., three to
four plants from each clone per OTC) were harvested for
analysis of aboveground biomass. The remaining plants in
each OTC were measured during the second growing season
and harvested on December 8--12, 1994. For both 1993 and
1994 harvests, leaves, branches and stems were oven dried at
80 °C for 3--7 days and weighed. All fallen leaves per OTC
were collected, dried and used for determination of total leaf
biomass. Because biomass data for 2-year-old stems are not yet
available, average biomass per clone per treatment was estimated at the end of the first year using the average stem volume
index (calculated from height and diameter measurements) of
all plants. Total leaf biomass per clone and per treatment at the
end of the second growing season was estimated from total
stem volumes. Total number of branches per plant was determined at the times of the 1993 and 1994 harvests.
Leaf nitrogen analysis and C/N ratio
In September 1993 and August and September 1994, several
leaves were sampled from five plants per clone per treatment
for analysis of total nitrogen content by the micro-Kjeldahl
GROWTH AND PRODUCTIVITY OF POPLAR IN ELEVATED CO2
63
technique. Five replicative measurements were made per sample.
The carbon to nitrogen ratio (C/N) was determined for
leaves of both treatments from the corresponding data on
biomass and nitrogen content assuming that 1 g dry weight =
0.45 g C (Larcher 1980).
Statistical treatment of data
A one-way or two-way analysis of variance (ANOVA) was
used to test significance of CO2 treatment and clone, as well as
interactions between these factors. By including chamber
within CO2 treatment as the experimental unit, between chamber variation could be accounted for in the analysis. Tukey’s
multiple range test or confidence interval test at P = 0.05 or
0.01 followed each ANOVA. A two-sample Student’s t-test
was performed on phenological observations (at P = 0.05).
Results
Seasonal evolution of height and leaf area index
Treatment differences in average plant height were small in the
middle of the first season, but by the end of the first growing
season, heights of clones Beaupré and Robusta were 14 and
17% greater, respectively, in the elevated CO2 treatment than
in the ambient CO2 treatment (P < 0.05) (Figure 1, top). At the
end of the first growing season, clone Beaupré was significantly taller (P < 0.01) than clone Robusta in both CO2 treatments. By the end of the second growing season, however, the
only significant clonal difference in plant height was in the
ambient CO2 treatment. At this time, clones Beaupré and
Robusta were 4.85 and 4.30 m in height, respectively, in the
ambient CO2 treatment (Figure 1, bottom). Although there
were no clonal differences in plant height in the elevated CO2
treatment at the end of the second growing season, Beaupré
and Robusta plants were 7 and 18% taller, respectively, in the
elevated CO2 treatment than in the ambient CO2 treatment (P
< 0.05). For clone Beaupré, the relative stimulation of plant
height growth by elevated CO2 was less in the second year than
in the first year, whereas it was nearly 17% in both years for
clone Robusta. For both clones and both treatments, plant
height more than doubled in the second year compared with
the first year. The difference in average height values at the
onset of the second year compared with the end of the first year
(Figure 1) was caused by the harvest of half of the plants in
each OTC at the end of the first year.
Leaf area index development generally showed the same
trend for both clones during both years, except for the later
start in the establishment year (Figure 2). In the first year, the
LAI of clone Beaupré was more than twice that of clone
Robusta in both CO2 treatments (Figure 2, top). The elevated
CO2 treatment significantly increased the LAI of clone Beaupré (P < 0.05) in both years. The larger CO2-induced increase
in LAI of clone Beaupré in the second year than in the first year
was the result of a low LAI in the ambient treatment in the
second year (Figure 2, bottom). The elevated CO2 treatment
had no significant effect on the LAI of clone Robusta at the end
of the first or second year (P < 0.05) (Figure 2, bottom).
Figure 1. Time course of average plant height with time during the first
(top panel) and second (bottom panel) growing season of poplar clones
Beaupré (triangles) and Robusta (squares) grown in open-top chambers in ambient or elevated atmospheric CO2. Solid lines and open
symbols represent the ambient treatment; dotted lines and filled symbols represent the elevated treatment. Fine vertical lines represent the
standard error of the mean (15 replications in the first year versus eight
replications in the second year).
Figure 2. Time course of leaf area index with time during the first (top
panel) and second (bottom panel) growing season of poplar clones
Beaupré (triangles) and Robusta (squares) grown in open-top chambers in ambient or elevated atmospheric CO2. Solid lines and open
symbols represent the ambient treatment; dotted lines and filled symbols represent the elevated treatment.
64
CEULEMANS, SHAO, JIANG AND KALINA
By the end of the second growing season, we had collected
over 55% more total leaf biomass in the OTCs providing the
elevated CO2 treatment than in the OTCs providing the ambient CO2 treatment. We calculated that the elevated CO2 treatment resulted in increases in total leaf biomass of 36 and 49%
for clones Beaupré and Robusta, respectively (Table 1). Thus,
although the LAI of clone Robusta was not significantly increased in the elevated CO2 treatment, its total leaf biomass
increased by nearly 50%, suggesting a large decrease in specific leaf area.
Bud phenology
The elevated CO2 treatment had no significant effects on average bud set dates, except at the end of the first year when bud
set in clone Robusta was significantly (P < 0.01) advanced by
4 days in the elevated CO2 treatment (Table 2). Although there
was no significant treatment effect on terminal bud set date in
clone Beaupré (Table 2), we observed considerable variation
among individual plants. For example, at the end of the first
year, the first Beaupré and Robusta plants in the elevated CO2
treatment set bud 20 and 9 days earlier, respectively, than in the
ambient CO2 treatment. Lateral branches set bud more than
1 month before the terminal shoot, and bud set of lateral
branches occurred 10 days earlier in clone Beaupré than in
clone Robusta (Table 2). Although a difference in bud set dates
of nearly 20 days was observed between the two clones at the
end of the first growing season (September 10 for clone Beaupré and October 1 for clone Robusta), no significant (P < 0.05)
clonal differences were observed at the end of the second
growing season.
Number and biomass of branches
Because of the small number of sylleptic side branches produced during the first year and the error involved in counting
the small branches of clone Robusta, we likely overestimated
the effect of elevated CO2 on small branch production (Table 3). After two growing seasons, the elevated CO2 treatment
caused a significant (P < 0.01) increase (21--26%) in total
number of branches produced by each clone. The elevated CO2
treatment enhanced the production of major proleptic branches
more than the production of smaller, sylleptic side shoots (data
not shown). The production of these major proleptic branches,
which only appear after the first growing season (Ceulemans
et al. 1990), accounts for the increase in total branch biomass
Table 1. Nitrogen concentration (% dry weight), total biomass (gDW plant −1), total nitrogen content (g plant −1) and C/N ratio of leaves of poplar
clones Beaupré and Robusta grown in open-top chambers in ambient or elevated CO2. Leaf nitrogen concentration data from two different sampling
dates in the second year (i.e., August and September 1994) are shown, as well as overall mean values for the first and second year. Data on total
leaf biomass and leaf nitrogen content are for the end of the second year and are expressed perplant. Values within parenthesis represent standard
error of the mean.
Beaupré
Robusta
Ambient
Elevated
Ambient
Elevated
Leaf nitrogen concentration (% dry weight)
Overall mean, first year
August, second year
September, second year
Overall mean, second year
1.53 (0.12)
1.56 (0.21)
2.12 (0.11)
1.84 (0.23)
1.19 (0.12)
1.07 (0.07)
1.30 (0.05)
1.19 (0.06)
1.79 (0.06)
1.62 (0.21)
2.11 (0.05)
1.86 (0.16)
1.23 (0.17)
1.25 (0.07)
1.81 (0.05)
1.53 (0.14)
Leaf biomass and leaf nitrogen content
Total leaf DW per plant (g)
Total leaf N content per plant (g)
C/N ratio of leaves
235 (84)
4.32 (1.64)
24.5 (9.9)
319 (39)
3.79 (0.50)
37.8 (5.4)
169 (60)
3.14 (1.15)
24.2 (9.7)
250 (41)
3.83 (0.72)
29.4 (5.9)
Table 2. Average bud set dates for poplar clones Beaupré and Robusta grown in open-top chambers in ambient or elevated CO2. Data from the ends
of the first and second growing season are shown; all numbers are days of the year. Mean valuesof 15 individual plants per clone per treatment in
the first year versus eight individual plants during the second year are presented. Values within parenthesis indicate standard error of the mean.
Beaupré
First year
Terminal bud set
Second year
Bud set of lateral branches
Terminal bud set
Robusta
Ambient
Elevated
Ambient
Elevated
274 (4)
October 1
274 (4)
October 1
253 (1)
September 10
249 (2)
September 6
250 (2)
September 7
296 (9)
October 23
249 (4)
September 6
293 (5)
October 20
260 (4)
September 17
295 (8)
October 22
260 (4)
September 17
292 (8)
October 19
GROWTH AND PRODUCTIVITY OF POPLAR IN ELEVATED CO2
65
Table 3. Total number of branches (per plant) of poplar clones Beaupré and Robusta during twogrowing seasons in open-top chambers in ambient
or elevated CO2. The number of branches was determined at the end of each growing season and includes small (sylleptic) as well as larger
(proleptic) branches. Mean values of 15 replications (first year) versus eight replications (second year) are presented. Values within parenthesis
represent standard error of the mean.
Beaupré
First year
Second year
Robusta
Ambient
Elevated
Ambient
Elevated
9
18.3 (1.8)
19
23.0 (2.6)
1
19.3 (2.4)
5
23.3 (2.6)
during the second year in the elevated CO2 treatment (Figure 3).
Figure 3 depicts the total branch dry weight per plant produced during the first and second growing seasons in the
ambient and elevated CO2 treatments. In both clones and both
years, there was a significant (P < 0.01) increase in branch
biomass per plant. The increase in total branch biomass caused
by the elevated CO2 treatment was proportionally larger for
clone Robusta (108%), which had fewer branches and smaller
total branch biomass, than for clone Beaupré (Table 3, Figure 3). In both clones, the stimulation of branch biomass by
elevated CO2 was greater in the second year than in the first
year. Absolute values of total branch biomass ranged from 3 to
9 g after 1 year and amounted to 80 to 190 g after 2 years of
growth.
Figure 4. Total stem volume (per plant) of poplar clones Beaupré (left)
and Robusta (right) at the end of the second growing season in opentop chambers supplied with ambient (open bars) or elevated (shaded
bars) CO2. Fine vertical lines represent standard error of the mean
(eight replications per clone).
Stem volume and biomass
We used total stem volume production per plant (or per OTC)
to estimate overall plant productivity. After 2 years of growth
in the presence of elevated CO2, we observed significant increases (P < 0.01) in stem volume per plant of 43 and 58% in
clones Beaupré and Robusta, respectively (Figure 4). The
increased stem volume production in the elevated CO2 treatment was explained not only by stimulated height growth but
also by increased stem diameters. We also observed significant
(P < 0.01) clonal differences in stem volume production per
plant. During both growing seasons and in both CO2 treatments, clone Beaupré had significantly (P < 0.01) greater stem
volume production than clone Robusta (2.5 versus 2.0 dm3 per
plant).
At the end of the first year, there was a significant clonal
difference (P < 0.01) in total biomass production (stem +
branches + leaves). Total biomass production of clone Beaupré
was 103 g in the ambient CO2 treatment versus 128 g in the
elevated CO2 treatment. The corresponding values for clone
Robusta were 48 and 66 g.
Nitrogen content of leaves
Figure 3. Total dry weight of branches (per plant) produced during the
first (shaded bar) and second (open bars) growing season by poplar
clones Beaupré (left) and Robusta (right) grown in ambient or elevated
atmospheric CO2. Total branch dry weight is presented on a logarithmic scale and expressed per plant. Fine vertical lines represent standard error of the mean (15 replications in the first year versus eight
replications in the second year).
The elevated CO2 treatment significantly decreased leaf nitrogen concentration (1.2 versus 1.8% of dry weight) in both
clones (Table 1) (cf. Ceulemans et al. 1995). Differences in
mean percent nitrogen concentration were not significant (P <
0.05) between growing seasons, except for clone Robusta in
the elevated CO2 treatment. During both years, total nitrogen
content of the leaves (i.e., total amount of aboveground nitrogen in leaf material) was not significantly decreased by the
elevated CO2 treatment in clone Beaupré (Table 1). In clone
Robusta, the total leaf nitrogen content decreased in the elevated CO2 treatment during the first year, but increased by 22%
in the second year. The foliar C/N ratio significantly increased
in both clones and both years (Table 1). The elevated CO2
treatment had little effect on the total amount of nitrogen in the
plant (leaves + stems + branches) in the first year (−7% for
clone Beaupré and +8% for clone Robusta).
66
CEULEMANS, SHAO, JIANG AND KALINA
Discussion
The two poplar clones exhibited different responses to elevated
atmospheric CO2, and there was an interaction between CO2
response and growing season, as has also been found in sour
orange trees (Idso et al. 1991). Thus, the concept of response
specificity among tree genera to an increase in atmospheric
CO2, as suggested by Mousseau and Enoch (1989) and El
Kohen et al. (1993), might also hold true within genera.
Both clones responded positively to elevated CO2 with an
increase in stem volume. The increase was larger in the second
year than in the first year indicating that the stimulation by
elevated CO2 is affected by plant age or the duration of exposure, or both. The slow-growing clone Robusta was more
responsive to the elevated CO2 treatment than the fast-growing
clone Beaupré as indicated by the larger increases in total
branch biomass, total leaf biomass and stem volume (Table 4).
The increase in stem volume in clone Beaupré was primarily
associated with increases in stem diameter, whereas the increase in stem volume in clone Robusta was primarily associated with increases in stem height (18%). Stimulated height
growth in response to elevated CO2 is in agreement with
previous observations on seedlings of several woody plants
(Eamus and Jarvis 1989, Radoglou and Jarvis 1990, Brown
1991, Norby et al. 1992, Duff et al. 1994). We have previously
shown that, in both clones, the stimulatory effect of elevated
CO2 on first-year height growth was caused by an increase in
internode length (i.e., enhanced stem elongation) and not by an
increase in the number of internodes produced (Ceulemans et
al. 1995).
Although net photosynthesis per unit leaf area was significantly increased in both clones in the elevated CO2 treatment
(Ceulemans et al. 1995), there was a large clonal difference
with respect to the effects of CO2 enrichment on total leaf area.
In response to the elevated CO2 treatment, clone Beaupré
displayed a significantly higher LAI than clone Robusta. In the
first and second years, the elevated CO2 treatment increased
LAI of clone Beaupré by 18 and 48%, respectively, whereas
the increases in total leaf biomass were only 4 and 36%,
respectively, suggesting a large decrease in specific leaf area in
the elevated CO2 treatment. The decrease in specific leaf area
was reflected in a decreased total N content of the leaves of
clone Beaupré in the elevated CO2 treatment.
Clone Robusta exhibited a small but significant increase
(8%) in LAI in response to elevated CO2 that remained constant during both growing seasons. Similar findings have been
reported for sweet chestnut (El Kohen et al. 1992, 1993) and
sour orange (Idso et al. 1991). The 8% increase in LAI observed in the middle of the first growing season in the elevated
CO2 treatment was reflected in a similar increase in total leaf
biomass by the end of the growing season (Table 4). However,
in the second year, clone Robusta produced much more leaf
biomass (reflected in an increase in total leaf N content per
plant) without an accompanying increase in leaf area, which
led to a significant reduction in overall specific leaf area (cf.
Oberbauer et al. 1985, Reekie and Bazzaz 1989). Reductions
in specific leaf area are generally ascribed to increased leaf
thickness (Mousseau and Enoch 1989) or foliar carbohydrate
accumulation (Wong 1990), or both (Jolliffe and Ehret 1985).
For both clones, the woody biomass produced per unit of leaf
biomass (Table 2) or per unit of leaf area (data not shown)
significantly increased. This increase was also reflected in the
leaf weight ratio, which decreased by 14 and 20% in clones
Beaupré and Robusta, respectively (Ceulemans et al. 1995).
Thus, in the elevated CO2 treatment, the slow-growing clone
became relatively more efficient in terms of the amount of
biomass produced per unit leaf than the fast-growing clone;
however, the fast-growing clone showed a more pronounced
decrease in specific leaf area in response to CO2 enrichment
than the slow-growing clone.
The elevated CO2 treatment induced large increases in the
biomass and number of branches (Table 4) (cf. Ceulemans et
al. 1990, Ceulemans et al. 1995). Large increases in branch
biomass in response to elevated CO2 have been reported for
sour orange trees (Idso et al. 1991). Idso et al. (1991) reported
that orange trees produced fourth-, fifth- and sixth-order
branches 2.5 years after exposure to elevated atmospheric CO2
conditions, whereas trees in the ambient treatment had no
branches above the third order. In contrast, in eucalypts, elevated CO2 treatment did not affect branch biomass but caused
large increases in stem and root biomass (Duff et al. 1994).
We have previously shown that elevated CO2 delays bud
Table 4. Relative difference (percent) between the elevated and ambient CO2 treatments for a number of aboveground growth and developmental
characteristics of poplar clones Beaupré and Robusta after 1 and 2 years of growth in open-topchambers. All differences are significant (per clone
per year), unless followed by ns.
Beaupré
Final plant height
Number of branches
Total biomass of branches
Total biomass of leaves
Leaf area index
Total nitrogen content of leaves
C/N ratio of leaves
Stem volume index
Stem volume
Robusta
First year
Second year
First year
Second year
+ 14
+ 111
+ 38
+ 4 ns
+ 18
− 19
+ 29
+ 7 ns
+ 26
+ 81
+ 36
+ 48
− 12 ns
+ 54
+ 11
+ 43
+ 17
(+ 400)
+ 58
+ 8 ns
+ 8 ns
− 25
+ 27
+ 18
+ 21
+ 108
+ 49
+ 8 ns
+ 22
+ 21
+ 4 ns
+ 58
GROWTH AND PRODUCTIVITY OF POPLAR IN ELEVATED CO2
burst by 2 to 5 days in clone Beaupré, whereas the treatment
has no significant effect on bud phenology in clone Robusta
(Ceulemans et al. 1995). Although no temperature differences
were observed between OTCs with different CO2 treatments,
Beuker (1994) suggested that global warming would result
primarily in important differences in leaf phenology and the
timing of bud burst, at least in coniferous plant species. At the
end of the first year, bud set of clone Robusta was advanced by
4 days in the elevated CO2 treatment. Similar findings have
been reported for sweet chestnut (Mousseau and Enoch 1989)
and birch (Evans and Lee 1993). We did not observe any
significant treatment differences in the timing of bud set for
branches or the current terminal leader. Gunderson et al.
(1993) has suggested that elevated CO2 effects on bud phenology are dependent on species or interactions of CO2 with
temperature, or both.
We conclude that both clones respond positively to elevated
CO2 concentrations. The CO2-induced responses of clone
Beaupré included increased investment in branch and leaf
biomass that resulted in a significantly increased leaf area
index. The CO2-induced responses of the slow-growing clone
Robusta included an increase in height growth and increased
investment in branch biomass and total leaf N content; however, these increases were not reflected in a higher LAI.
Acknowledgments
This research forms part of the European ECOCRAFT network, supported by the EC R and D Environment Program (Contract No. EV5VCT92-0127) and coordinated by the University of Edinburgh,
Scotland. Further support was provided by the Belgian National Fund
for Scientific Research (Brussels) and the Special Research Fund of
the University of Antwerpen (UIA). We gratefully acknowledge
K. Brouwers and N. Calluy for nitrogen analysis, F. Kockelbergh and
G. Heiler for technical assistance, and K. Bortier, L. Van Praet and B.
Van Staeyen for help with biomass determinations. RC is a Senior
Research Associate of the Belgian NFWO.
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© 1996 Heron Publishing----Victoria, Canada
First- and second-year aboveground growth and productivity of two
Populus hybrids grown at ambient and elevated CO2
R. CEULEMANS,1 B. Y. SHAO,1 X. N. JIANG2 and J. KALINA3
1
Department of Biology, University of Antwerpen (UIA), Universiteitsplein 1, B-2610 Wilrijk, Belgium
2
Experimental Center of Forest Biology, Beijing Forestry University, 100083 Beijing, Peoples Republi
c of China
3
Academy of Sciences of the Czech Republic, Institute of Landscape Ecology, Department of Ecological
Physiology of Forest Trees, CS-60300 Brno,
Czech Republic
Received March 2, 1995
Summary Two hybrid poplar (Populus) clones (the fastgrowing clone Beaupré (P. trichocarpa Torr. and Gray × P. deltoides Bartr. ex Marsh.) and the slow-growing clone Robusta
(P. deltoides Bartr. ex Marsh. × P. nigra L.)) were grown from
hardwood cuttings for one or two growing seasons (1993-1994) in either ambient or elevated (= ambient + 350 µmol
mol −1) CO2 in open-top chambers at the University of Antwerpen. Both clones responded positively to the elevated CO2
treatment with increased stem volume and aboveground
biomass production; however, the clones exhibited different
response strategies to the elevated CO2 treatment, and the
responses varied with cutting age and duration of exposure.
Clone Beaupré responded to the elevated CO2 treatment with
increases in leaf area and leaf area index during both the first
and second growing seasons, but little increase in height
growth. Clone Robusta exhibited increased height growth, leaf
biomass and total leaf nitrogen content in response to elevated
CO2, but no increase in leaf area index. The elevated CO2
treatment increased the total number of branches and total
branch biomass in both clones during both growing seasons.
At the end of the first growing season, woody stem biomass of
the fast- and slow-growing clones was increased by 38 and
55%, respectively. At the end of the second growing season,
stem volume was increased by 43% in clone Beaupré and by
58% in clone Robusta. The increase in stem volume was a result
of the stimulation of both height and diameter growth in the
slow-growing clone, whereas only height growth was stimulated in the fast-growing clone. In the fall of the first growing
season, the average date of bud set in clone Robusta was
advanced by 4 days in the elevated CO2 treatment; there were
no other significant effects of the elevated CO2 treatment on
bud set. The elevated CO2 treatment enhanced leaf C/N ratios
in both clones in both years.
Keywords: branches, leaf area index, nitrogen content, poplar,
volume index.
Introduction
The growth of deciduous trees often increases by about 30% in
response to elevated concentrations of atmospheric CO2,
whereas the overall mean effect of elevated CO2 on total
aboveground biomass production (or total gross photosynthesis) ranges from 0.5 to 15% (Strain 1987, Norby 1989, Eamus
and Jarvis 1989, Mousseau and Saugier 1992, Ceulemans and
Mousseau 1994). However, among different tree genera as
well as among different species and genotypes within the same
genus, responses to elevated CO2 vary greatly (Norby et al.
1986, O’Neill et al. 1987, Radoglou and Jarvis 1990, Rogers
et al. 1994, Ceulemans and Mousseau 1994). For example, El
Kohen et al. (1993) observed that elevated CO2 had no effect
on leaf area of sweet chestnut, whereas it increased total leaf
area of beech plants. Duff et al. (1994) found significant
differences in the growth rates of two closely related eucalypt
species of northern Australia in response to CO2 enrichment.
Because tree responses to increasing atmospheric CO2 concentrations appear to be species- and genotype-specific, there
is an urgent need to obtain more detailed information on the
likely consequences of the predicted global CO2 change on
growth, development and productivity of forest trees. Accordingly, the ECOCRAFT research network, consisting of more
than 12 European university laboratories and research institutes, was established in 1990 with the overall objective of
examining the impacts of increasing atmospheric CO2 concentration and temperature on European forests. Within the framework of this network, we have studied the effects of elevated
atmospheric CO2 concentrations on the growth, physiology
and development of two genotypes of poplar (Populus). Poplar
species and hybrids were used because they are planted as high
productivity, short-rotation tree crops (e.g., Ceulemans et al.
1987, 1993) and generally show a large positive response to
short-term CO2 enrichment (Gaudillère and Mousseau 1989,
Radoglou and Jarvis 1990, Brown 1991) under controlled
environment conditions.
To examine the long-term effects of an increase in atmospheric CO2 concentration on two Populus clones, Beaupré
62
CEULEMANS, SHAO, JIANG AND KALINA
(P. trichocarpa Torr. and Gray × P. deltoides Bartr. ex Marsh.)
and Robusta (P. deltoides Bartr. ex Marsh. × P. nigra L.),
differing in growth performance, we exposed clonal cuttings to
elevated atmospheric CO2 concentrations for two growing
seasons in open-top chambers. Clone Beaupré is a fast-growing clone (Ceulemans et al. 1987, Radoglou and Jarvis 1990,
Barigah et al. 1994) and clone Robusta is a slow-growing clone
(Radoglou and Jarvis 1990, Barigah et al. 1994). The clones
exhibited different responses to elevated CO2 treatment, which
varied with cutting age and duration of exposure.
al. 1993), and then the individual leaf areas were summed to
obtain the total leaf area per plant. In the second year, only
dimensions of individual leaves on the current terminal leader
were measured, and branch dimensions and allometric relationships of branch diameter versus leaf area (Ceulemans et al.
1993) were used to determine total leaf area per plant. Leaf
area indices of each clone and each treatment were obtained by
dividing the total leaf area of 15 plants (first year) or eight
plants (second year) by the ground area (7 m2) of each OTC,
assuming no interclonal competition within each OTC.
Phenological observations
Materials and methods
Plant materials and planting pattern
Two hybrid poplar clones, the fast-growing interamerican
clone Beaupré and the slow-growing euramerican clone
Robusta, were raised from clonal hardwood cuttings (25 cm
long) in four open-top chambers (OTCs) at the University of
Antwerpen, Belgium. On April 22, 1993, the cuttings, 15 per
OTC (i.e., 7 to 8 plants of each clone), were planted in a circle
at a spacing of 0.6 m. The distance between adjacent OTCs
ranged from 8 to 10 m, and to reduce the boundary effect, each
OTC was surrounded by 19 plants. Before planting, the heavy
clay soil was excavated from each OTC to a depth of 50 cm and
replaced with fertile, black horticultural soil. Each OTC was
manually weeded, and all plants were automatically drip irrigated throughout the two growing seasons. Because nutrient
conditions were near optimal at the start of the experiment,
fertilizer was only applied once during the first growing season
and three times during the second growing season.
Open-top chamber design
Each decagonal OTC (3 m in diameter and 6 m in height) was
made of 1-m wide Plexiglas sheets and had a usable ground
area of 7 m2. Incoming chamber air was supplied by large
ventilators (S and P, CBM 320-65, Spain) at a rate of about
6500 m3 h −1, i.e., about two air volume changes per minute. Air
distribution within the OTC was effected through a flexible
spiroid pipe attached to a perforated polythene annulus 1 m
above the ground. Two OTCs provided a control treatment at
ambient atmospheric CO2 (about 350 µmol mol −1), and the
other two OTCs provided an elevated CO2 treatment at ambient
+ 350 µmol mol −1 (about 700 µmol mol −1). Input of CO2 was
controlled by a gas mass flowmeter (Model 5851E, Brooks
Instruments, Rosemount, The Netherlands) and was supplied
24 h per day from April 1993 until early November 1993 and
from mid-March 1994 until early November 1994. No CO2
enrichment was supplied from November 1993 to March 17,
1994.
Nondestructive height and leaf area measurements
Total plant height was monitored throughout each growing
season until November. Leaf area index (LAI) was determined
nondestructively for each clone and each treatment. In the first
year, individual leaf area was estimated by means of allometric
relations between leaf dimensions and leaf area (Ceulemans et
From September onward, observations on bud set and leaf fall
were made per clone and per treatment. Dates of bud set were
determined for terminal shoots as well as for branches (second
year). For all phenological observations, mean values (± SE)
of all plants (15 and eight plants per clone and per treatment in
the first and second year, respectively) were calculated.
Stem volume determinations
At the end of the first growing season, stem diameters at the
top and bottom of each plant were measured (in two perpendicular directions) with a caliper. Stem volume index was
estimated for each plant as (π/3)H(R12 + R1R2 + R22), where R1
and R2 are the radii at the bottom and the top of the stem,
respectively, and H is total plant height. At the end of the
second year, stem diameters of all harvested plants were measured at 1-m intervals. For each 1-m stem segment, the volume
was calculated based on the formula for a truncated cone as
above, but where R1 and R2 are the radii at the base and the top
of each stem segment, respectively, and H is the length of the
segment. Total stem volume per plant was obtained by summing the volumes of all individual stem segments (Causton
1985).
Destructive biomass measurements
At the end of November 1993, half of the plants (i.e., three to
four plants from each clone per OTC) were harvested for
analysis of aboveground biomass. The remaining plants in
each OTC were measured during the second growing season
and harvested on December 8--12, 1994. For both 1993 and
1994 harvests, leaves, branches and stems were oven dried at
80 °C for 3--7 days and weighed. All fallen leaves per OTC
were collected, dried and used for determination of total leaf
biomass. Because biomass data for 2-year-old stems are not yet
available, average biomass per clone per treatment was estimated at the end of the first year using the average stem volume
index (calculated from height and diameter measurements) of
all plants. Total leaf biomass per clone and per treatment at the
end of the second growing season was estimated from total
stem volumes. Total number of branches per plant was determined at the times of the 1993 and 1994 harvests.
Leaf nitrogen analysis and C/N ratio
In September 1993 and August and September 1994, several
leaves were sampled from five plants per clone per treatment
for analysis of total nitrogen content by the micro-Kjeldahl
GROWTH AND PRODUCTIVITY OF POPLAR IN ELEVATED CO2
63
technique. Five replicative measurements were made per sample.
The carbon to nitrogen ratio (C/N) was determined for
leaves of both treatments from the corresponding data on
biomass and nitrogen content assuming that 1 g dry weight =
0.45 g C (Larcher 1980).
Statistical treatment of data
A one-way or two-way analysis of variance (ANOVA) was
used to test significance of CO2 treatment and clone, as well as
interactions between these factors. By including chamber
within CO2 treatment as the experimental unit, between chamber variation could be accounted for in the analysis. Tukey’s
multiple range test or confidence interval test at P = 0.05 or
0.01 followed each ANOVA. A two-sample Student’s t-test
was performed on phenological observations (at P = 0.05).
Results
Seasonal evolution of height and leaf area index
Treatment differences in average plant height were small in the
middle of the first season, but by the end of the first growing
season, heights of clones Beaupré and Robusta were 14 and
17% greater, respectively, in the elevated CO2 treatment than
in the ambient CO2 treatment (P < 0.05) (Figure 1, top). At the
end of the first growing season, clone Beaupré was significantly taller (P < 0.01) than clone Robusta in both CO2 treatments. By the end of the second growing season, however, the
only significant clonal difference in plant height was in the
ambient CO2 treatment. At this time, clones Beaupré and
Robusta were 4.85 and 4.30 m in height, respectively, in the
ambient CO2 treatment (Figure 1, bottom). Although there
were no clonal differences in plant height in the elevated CO2
treatment at the end of the second growing season, Beaupré
and Robusta plants were 7 and 18% taller, respectively, in the
elevated CO2 treatment than in the ambient CO2 treatment (P
< 0.05). For clone Beaupré, the relative stimulation of plant
height growth by elevated CO2 was less in the second year than
in the first year, whereas it was nearly 17% in both years for
clone Robusta. For both clones and both treatments, plant
height more than doubled in the second year compared with
the first year. The difference in average height values at the
onset of the second year compared with the end of the first year
(Figure 1) was caused by the harvest of half of the plants in
each OTC at the end of the first year.
Leaf area index development generally showed the same
trend for both clones during both years, except for the later
start in the establishment year (Figure 2). In the first year, the
LAI of clone Beaupré was more than twice that of clone
Robusta in both CO2 treatments (Figure 2, top). The elevated
CO2 treatment significantly increased the LAI of clone Beaupré (P < 0.05) in both years. The larger CO2-induced increase
in LAI of clone Beaupré in the second year than in the first year
was the result of a low LAI in the ambient treatment in the
second year (Figure 2, bottom). The elevated CO2 treatment
had no significant effect on the LAI of clone Robusta at the end
of the first or second year (P < 0.05) (Figure 2, bottom).
Figure 1. Time course of average plant height with time during the first
(top panel) and second (bottom panel) growing season of poplar clones
Beaupré (triangles) and Robusta (squares) grown in open-top chambers in ambient or elevated atmospheric CO2. Solid lines and open
symbols represent the ambient treatment; dotted lines and filled symbols represent the elevated treatment. Fine vertical lines represent the
standard error of the mean (15 replications in the first year versus eight
replications in the second year).
Figure 2. Time course of leaf area index with time during the first (top
panel) and second (bottom panel) growing season of poplar clones
Beaupré (triangles) and Robusta (squares) grown in open-top chambers in ambient or elevated atmospheric CO2. Solid lines and open
symbols represent the ambient treatment; dotted lines and filled symbols represent the elevated treatment.
64
CEULEMANS, SHAO, JIANG AND KALINA
By the end of the second growing season, we had collected
over 55% more total leaf biomass in the OTCs providing the
elevated CO2 treatment than in the OTCs providing the ambient CO2 treatment. We calculated that the elevated CO2 treatment resulted in increases in total leaf biomass of 36 and 49%
for clones Beaupré and Robusta, respectively (Table 1). Thus,
although the LAI of clone Robusta was not significantly increased in the elevated CO2 treatment, its total leaf biomass
increased by nearly 50%, suggesting a large decrease in specific leaf area.
Bud phenology
The elevated CO2 treatment had no significant effects on average bud set dates, except at the end of the first year when bud
set in clone Robusta was significantly (P < 0.01) advanced by
4 days in the elevated CO2 treatment (Table 2). Although there
was no significant treatment effect on terminal bud set date in
clone Beaupré (Table 2), we observed considerable variation
among individual plants. For example, at the end of the first
year, the first Beaupré and Robusta plants in the elevated CO2
treatment set bud 20 and 9 days earlier, respectively, than in the
ambient CO2 treatment. Lateral branches set bud more than
1 month before the terminal shoot, and bud set of lateral
branches occurred 10 days earlier in clone Beaupré than in
clone Robusta (Table 2). Although a difference in bud set dates
of nearly 20 days was observed between the two clones at the
end of the first growing season (September 10 for clone Beaupré and October 1 for clone Robusta), no significant (P < 0.05)
clonal differences were observed at the end of the second
growing season.
Number and biomass of branches
Because of the small number of sylleptic side branches produced during the first year and the error involved in counting
the small branches of clone Robusta, we likely overestimated
the effect of elevated CO2 on small branch production (Table 3). After two growing seasons, the elevated CO2 treatment
caused a significant (P < 0.01) increase (21--26%) in total
number of branches produced by each clone. The elevated CO2
treatment enhanced the production of major proleptic branches
more than the production of smaller, sylleptic side shoots (data
not shown). The production of these major proleptic branches,
which only appear after the first growing season (Ceulemans
et al. 1990), accounts for the increase in total branch biomass
Table 1. Nitrogen concentration (% dry weight), total biomass (gDW plant −1), total nitrogen content (g plant −1) and C/N ratio of leaves of poplar
clones Beaupré and Robusta grown in open-top chambers in ambient or elevated CO2. Leaf nitrogen concentration data from two different sampling
dates in the second year (i.e., August and September 1994) are shown, as well as overall mean values for the first and second year. Data on total
leaf biomass and leaf nitrogen content are for the end of the second year and are expressed perplant. Values within parenthesis represent standard
error of the mean.
Beaupré
Robusta
Ambient
Elevated
Ambient
Elevated
Leaf nitrogen concentration (% dry weight)
Overall mean, first year
August, second year
September, second year
Overall mean, second year
1.53 (0.12)
1.56 (0.21)
2.12 (0.11)
1.84 (0.23)
1.19 (0.12)
1.07 (0.07)
1.30 (0.05)
1.19 (0.06)
1.79 (0.06)
1.62 (0.21)
2.11 (0.05)
1.86 (0.16)
1.23 (0.17)
1.25 (0.07)
1.81 (0.05)
1.53 (0.14)
Leaf biomass and leaf nitrogen content
Total leaf DW per plant (g)
Total leaf N content per plant (g)
C/N ratio of leaves
235 (84)
4.32 (1.64)
24.5 (9.9)
319 (39)
3.79 (0.50)
37.8 (5.4)
169 (60)
3.14 (1.15)
24.2 (9.7)
250 (41)
3.83 (0.72)
29.4 (5.9)
Table 2. Average bud set dates for poplar clones Beaupré and Robusta grown in open-top chambers in ambient or elevated CO2. Data from the ends
of the first and second growing season are shown; all numbers are days of the year. Mean valuesof 15 individual plants per clone per treatment in
the first year versus eight individual plants during the second year are presented. Values within parenthesis indicate standard error of the mean.
Beaupré
First year
Terminal bud set
Second year
Bud set of lateral branches
Terminal bud set
Robusta
Ambient
Elevated
Ambient
Elevated
274 (4)
October 1
274 (4)
October 1
253 (1)
September 10
249 (2)
September 6
250 (2)
September 7
296 (9)
October 23
249 (4)
September 6
293 (5)
October 20
260 (4)
September 17
295 (8)
October 22
260 (4)
September 17
292 (8)
October 19
GROWTH AND PRODUCTIVITY OF POPLAR IN ELEVATED CO2
65
Table 3. Total number of branches (per plant) of poplar clones Beaupré and Robusta during twogrowing seasons in open-top chambers in ambient
or elevated CO2. The number of branches was determined at the end of each growing season and includes small (sylleptic) as well as larger
(proleptic) branches. Mean values of 15 replications (first year) versus eight replications (second year) are presented. Values within parenthesis
represent standard error of the mean.
Beaupré
First year
Second year
Robusta
Ambient
Elevated
Ambient
Elevated
9
18.3 (1.8)
19
23.0 (2.6)
1
19.3 (2.4)
5
23.3 (2.6)
during the second year in the elevated CO2 treatment (Figure 3).
Figure 3 depicts the total branch dry weight per plant produced during the first and second growing seasons in the
ambient and elevated CO2 treatments. In both clones and both
years, there was a significant (P < 0.01) increase in branch
biomass per plant. The increase in total branch biomass caused
by the elevated CO2 treatment was proportionally larger for
clone Robusta (108%), which had fewer branches and smaller
total branch biomass, than for clone Beaupré (Table 3, Figure 3). In both clones, the stimulation of branch biomass by
elevated CO2 was greater in the second year than in the first
year. Absolute values of total branch biomass ranged from 3 to
9 g after 1 year and amounted to 80 to 190 g after 2 years of
growth.
Figure 4. Total stem volume (per plant) of poplar clones Beaupré (left)
and Robusta (right) at the end of the second growing season in opentop chambers supplied with ambient (open bars) or elevated (shaded
bars) CO2. Fine vertical lines represent standard error of the mean
(eight replications per clone).
Stem volume and biomass
We used total stem volume production per plant (or per OTC)
to estimate overall plant productivity. After 2 years of growth
in the presence of elevated CO2, we observed significant increases (P < 0.01) in stem volume per plant of 43 and 58% in
clones Beaupré and Robusta, respectively (Figure 4). The
increased stem volume production in the elevated CO2 treatment was explained not only by stimulated height growth but
also by increased stem diameters. We also observed significant
(P < 0.01) clonal differences in stem volume production per
plant. During both growing seasons and in both CO2 treatments, clone Beaupré had significantly (P < 0.01) greater stem
volume production than clone Robusta (2.5 versus 2.0 dm3 per
plant).
At the end of the first year, there was a significant clonal
difference (P < 0.01) in total biomass production (stem +
branches + leaves). Total biomass production of clone Beaupré
was 103 g in the ambient CO2 treatment versus 128 g in the
elevated CO2 treatment. The corresponding values for clone
Robusta were 48 and 66 g.
Nitrogen content of leaves
Figure 3. Total dry weight of branches (per plant) produced during the
first (shaded bar) and second (open bars) growing season by poplar
clones Beaupré (left) and Robusta (right) grown in ambient or elevated
atmospheric CO2. Total branch dry weight is presented on a logarithmic scale and expressed per plant. Fine vertical lines represent standard error of the mean (15 replications in the first year versus eight
replications in the second year).
The elevated CO2 treatment significantly decreased leaf nitrogen concentration (1.2 versus 1.8% of dry weight) in both
clones (Table 1) (cf. Ceulemans et al. 1995). Differences in
mean percent nitrogen concentration were not significant (P <
0.05) between growing seasons, except for clone Robusta in
the elevated CO2 treatment. During both years, total nitrogen
content of the leaves (i.e., total amount of aboveground nitrogen in leaf material) was not significantly decreased by the
elevated CO2 treatment in clone Beaupré (Table 1). In clone
Robusta, the total leaf nitrogen content decreased in the elevated CO2 treatment during the first year, but increased by 22%
in the second year. The foliar C/N ratio significantly increased
in both clones and both years (Table 1). The elevated CO2
treatment had little effect on the total amount of nitrogen in the
plant (leaves + stems + branches) in the first year (−7% for
clone Beaupré and +8% for clone Robusta).
66
CEULEMANS, SHAO, JIANG AND KALINA
Discussion
The two poplar clones exhibited different responses to elevated
atmospheric CO2, and there was an interaction between CO2
response and growing season, as has also been found in sour
orange trees (Idso et al. 1991). Thus, the concept of response
specificity among tree genera to an increase in atmospheric
CO2, as suggested by Mousseau and Enoch (1989) and El
Kohen et al. (1993), might also hold true within genera.
Both clones responded positively to elevated CO2 with an
increase in stem volume. The increase was larger in the second
year than in the first year indicating that the stimulation by
elevated CO2 is affected by plant age or the duration of exposure, or both. The slow-growing clone Robusta was more
responsive to the elevated CO2 treatment than the fast-growing
clone Beaupré as indicated by the larger increases in total
branch biomass, total leaf biomass and stem volume (Table 4).
The increase in stem volume in clone Beaupré was primarily
associated with increases in stem diameter, whereas the increase in stem volume in clone Robusta was primarily associated with increases in stem height (18%). Stimulated height
growth in response to elevated CO2 is in agreement with
previous observations on seedlings of several woody plants
(Eamus and Jarvis 1989, Radoglou and Jarvis 1990, Brown
1991, Norby et al. 1992, Duff et al. 1994). We have previously
shown that, in both clones, the stimulatory effect of elevated
CO2 on first-year height growth was caused by an increase in
internode length (i.e., enhanced stem elongation) and not by an
increase in the number of internodes produced (Ceulemans et
al. 1995).
Although net photosynthesis per unit leaf area was significantly increased in both clones in the elevated CO2 treatment
(Ceulemans et al. 1995), there was a large clonal difference
with respect to the effects of CO2 enrichment on total leaf area.
In response to the elevated CO2 treatment, clone Beaupré
displayed a significantly higher LAI than clone Robusta. In the
first and second years, the elevated CO2 treatment increased
LAI of clone Beaupré by 18 and 48%, respectively, whereas
the increases in total leaf biomass were only 4 and 36%,
respectively, suggesting a large decrease in specific leaf area in
the elevated CO2 treatment. The decrease in specific leaf area
was reflected in a decreased total N content of the leaves of
clone Beaupré in the elevated CO2 treatment.
Clone Robusta exhibited a small but significant increase
(8%) in LAI in response to elevated CO2 that remained constant during both growing seasons. Similar findings have been
reported for sweet chestnut (El Kohen et al. 1992, 1993) and
sour orange (Idso et al. 1991). The 8% increase in LAI observed in the middle of the first growing season in the elevated
CO2 treatment was reflected in a similar increase in total leaf
biomass by the end of the growing season (Table 4). However,
in the second year, clone Robusta produced much more leaf
biomass (reflected in an increase in total leaf N content per
plant) without an accompanying increase in leaf area, which
led to a significant reduction in overall specific leaf area (cf.
Oberbauer et al. 1985, Reekie and Bazzaz 1989). Reductions
in specific leaf area are generally ascribed to increased leaf
thickness (Mousseau and Enoch 1989) or foliar carbohydrate
accumulation (Wong 1990), or both (Jolliffe and Ehret 1985).
For both clones, the woody biomass produced per unit of leaf
biomass (Table 2) or per unit of leaf area (data not shown)
significantly increased. This increase was also reflected in the
leaf weight ratio, which decreased by 14 and 20% in clones
Beaupré and Robusta, respectively (Ceulemans et al. 1995).
Thus, in the elevated CO2 treatment, the slow-growing clone
became relatively more efficient in terms of the amount of
biomass produced per unit leaf than the fast-growing clone;
however, the fast-growing clone showed a more pronounced
decrease in specific leaf area in response to CO2 enrichment
than the slow-growing clone.
The elevated CO2 treatment induced large increases in the
biomass and number of branches (Table 4) (cf. Ceulemans et
al. 1990, Ceulemans et al. 1995). Large increases in branch
biomass in response to elevated CO2 have been reported for
sour orange trees (Idso et al. 1991). Idso et al. (1991) reported
that orange trees produced fourth-, fifth- and sixth-order
branches 2.5 years after exposure to elevated atmospheric CO2
conditions, whereas trees in the ambient treatment had no
branches above the third order. In contrast, in eucalypts, elevated CO2 treatment did not affect branch biomass but caused
large increases in stem and root biomass (Duff et al. 1994).
We have previously shown that elevated CO2 delays bud
Table 4. Relative difference (percent) between the elevated and ambient CO2 treatments for a number of aboveground growth and developmental
characteristics of poplar clones Beaupré and Robusta after 1 and 2 years of growth in open-topchambers. All differences are significant (per clone
per year), unless followed by ns.
Beaupré
Final plant height
Number of branches
Total biomass of branches
Total biomass of leaves
Leaf area index
Total nitrogen content of leaves
C/N ratio of leaves
Stem volume index
Stem volume
Robusta
First year
Second year
First year
Second year
+ 14
+ 111
+ 38
+ 4 ns
+ 18
− 19
+ 29
+ 7 ns
+ 26
+ 81
+ 36
+ 48
− 12 ns
+ 54
+ 11
+ 43
+ 17
(+ 400)
+ 58
+ 8 ns
+ 8 ns
− 25
+ 27
+ 18
+ 21
+ 108
+ 49
+ 8 ns
+ 22
+ 21
+ 4 ns
+ 58
GROWTH AND PRODUCTIVITY OF POPLAR IN ELEVATED CO2
burst by 2 to 5 days in clone Beaupré, whereas the treatment
has no significant effect on bud phenology in clone Robusta
(Ceulemans et al. 1995). Although no temperature differences
were observed between OTCs with different CO2 treatments,
Beuker (1994) suggested that global warming would result
primarily in important differences in leaf phenology and the
timing of bud burst, at least in coniferous plant species. At the
end of the first year, bud set of clone Robusta was advanced by
4 days in the elevated CO2 treatment. Similar findings have
been reported for sweet chestnut (Mousseau and Enoch 1989)
and birch (Evans and Lee 1993). We did not observe any
significant treatment differences in the timing of bud set for
branches or the current terminal leader. Gunderson et al.
(1993) has suggested that elevated CO2 effects on bud phenology are dependent on species or interactions of CO2 with
temperature, or both.
We conclude that both clones respond positively to elevated
CO2 concentrations. The CO2-induced responses of clone
Beaupré included increased investment in branch and leaf
biomass that resulted in a significantly increased leaf area
index. The CO2-induced responses of the slow-growing clone
Robusta included an increase in height growth and increased
investment in branch biomass and total leaf N content; however, these increases were not reflected in a higher LAI.
Acknowledgments
This research forms part of the European ECOCRAFT network, supported by the EC R and D Environment Program (Contract No. EV5VCT92-0127) and coordinated by the University of Edinburgh,
Scotland. Further support was provided by the Belgian National Fund
for Scientific Research (Brussels) and the Special Research Fund of
the University of Antwerpen (UIA). We gratefully acknowledge
K. Brouwers and N. Calluy for nitrogen analysis, F. Kockelbergh and
G. Heiler for technical assistance, and K. Bortier, L. Van Praet and B.
Van Staeyen for help with biomass determinations. RC is a Senior
Research Associate of the Belgian NFWO.
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