Tree Physiology 21, 1279–1287
© 2001 Heron Publishing—Victoria, Canada
Effects of elevated carbon dioxide concentration and temperature on
needle growth, respiration and carbohydrate status in field-grown
Scots pines during the needle expansion period
TIANSHAN ZHA,1 AIJA RYYPPÖ,1 KAI-YUN WANG2 and SEPPO KELLOMÄKI1,3
1
University of Joensuu, Faculty of Forestry, P.O. Box 111, FIN-80101 Joensuu, Finland
2
Chendu Institute of Biology, Chinese Academy of Sciences, 416, 610041, Chendu, P.R. China
3
Author to whom correspondence should be addressed
Received January 8, 2001
Summary We determined effects of long-term elevation of
carbon dioxide concentration ([CO2 ]) and temperature on
growth, respiration and carbohydrate concentration in needles
of field-grown Scots pine (Pinus sylvestris L.) trees during the
needle expansion period. Sixteen 20-year-old Scots pine trees
were individually enclosed in closed-top, environmentally
controlled chambers for 4 years in one of four environments:
ambient conditions (CON); elevated [CO2 ] (EC); elevated
temperature (ET); and a combination of both (EC + ET). Needle growth, carbohydrate concentration and dark respiration
were measured at 3-day intervals throughout the needle expansion period. Dark respiration was partitioned into growth and
maintenance components by regressing specific respiration
rate against specific growth rate. In all treatments, growth, carbohydrate concentration and daily dark respiration rates of
needles followed a similar seasonal pattern throughout the
needle expansion period. Treatments EC, ET and EC + ET increased individual needle area and dry weight compared with
the CON treatment. Carbohydrate concentrations in needles
were increased by EC, but reduced by ET and EC + ET. Daily
respiration rates increased slightly in the early stage of needle
expansion and decreased gradually in the late stage when needles were exposed to EC, but increased consistently throughout
the growing period when needles were exposed to ET or EC +
ET. Partitioning of respiration into its two functional components showed that the growth respiration coefficient was unaffected by the treatments, whereas maintenance respiration was
reduced by EC but increased by ET and EC + ET. Maintenance
respiration was more sensitive to elevated temperature than
growth respiration. We conclude that the difference in respiration rates between expanding and expanded needles should be
taken into account when estimating the respiratory responses
of needles to elevated [CO2 ] and temperature.
Keywords: environment-controlled chamber, growth respiration, maintenance respiration, specific growth rate.
Introduction
Plant respiration accounts for a large proportion of carbon cycling in forest ecosystems and is a major determinant of net
primary production (Amthor 1989, Ryan et al. 1997). Both
CO2 concentration ([CO2]) and temperature are key variables
affecting plant growth, development and function, and both
have changed in the recent past and are predicted to increase in
the future. Increases in [CO2] and temperature could have
great effects on plant growth and physiology.
Much research is currently focused on respiratory responses
to rising atmospheric [CO2 ]. Studies of the effects of elevated
[CO2 ] on plant respiration rates have yielded conflicting results. Respiration rates are reported to increase (Gifford et al.
1985, Hrubec et al. 1985, Nijs et al. 1989, Thomas and Griffin
1994), decrease (Reuveni and Gale 1985, Bunce and Caulfield
1991, Baker et al. 1992, Wullschleger et al. 1992a, Teskey
1995, Jach and Ceulemans 2000) or remain unchanged (Curtis
et al. 1995) in response to atmospheric CO2 enrichment. Some
of the discrepancies among these studies may be attributed to
differences in species, plant development stage, leaf age and
carbohydrate concentration, length of exposure to elevated
[CO2 ], the basis used to express respiration rates, and artifacts
resulting from the methodology. Many atmospheric CO2 enrichment studies on woody plants have been restricted to seedlings and young trees grown under laboratory conditions
(Jarvis 1998, Saxe et al. 1998). However, seedling responses
may differ from those of mature trees (Mousseau and Saugier
1992), and responses obtained under laboratory conditions
may differ from those obtained under field conditions (Drake
1992). It is therefore necessary to investigate the respiratory
response of trees subjected to long-term elevated [CO2 ] in the
field.
A detailed understanding of the long-term effects of elevated [CO2 ] on dark respiration is necessary to model plant responses to climate change. The lack of a mechanistic understanding of the respiratory response to climate change has led
many researchers to partition respiration into functional categories (growth versus maintenance) or temporally distinct re-
1280
ZHA, RYYPPÖ, WANG AND KELLOMÄKI
sponses (direct versus indirect effects) (Ryan 1991, Wullschleger and Norby 1992, Kellomäki and Wang 1998). Dark
respiration rates can be altered as a result of a long-term acclimation response to elevated [CO2 ] (Wullschleger et al. 1994,
Norby et al. 1999) or through instantaneous changes in [CO2 ]
(Amthor 1991). Several authors have shown that a short-term
increase in [CO2 ] reversibly inhibits respiration rates (Wullschleger et al. 1994, Griffin et al. 1996, Jach and Ceulemans
2000), whereas small or no direct effects of rising atmospheric
[CO2 ] on tree-leaf respiration have been found in deciduous
forests (Amthor 2000).
Short-term increases in temperature enhance the dark respiration rates of tree leaves, typically in an exponential manner.
The degree to which leaf respiration changes with temperature
is highly variable, with temperature coefficient (Q10) values
ranging from 1.4 to 4.0 (Azcón-Bieto 1992), although generally Q10 = 2 (Kozlowski et al. 1991, Tjoelker et al. 1999). Leaf
respiration rates also depend on the degree of respiratory acclimation to changes in growth temperature. Downward shifts in
respiration acclimation to growth temperature are frequently
observed (Arnone and Körner 1997, Atkin et al. 2000, Gunderson et al. 2000, Will 2000); however, the interactive effects
of elevated [CO2 ] and temperature have not been closely studied (Ceulemans et al. 1999).
Our objective was to determine the effects of long-term exposure to elevated [CO2 ] and temperature on growth, respiration and carbohydrate status in needles of field-grown Scots
pines (Pinus sylvestris L.) during the needle expansion period.
The trees were about 20 years old and had been exposed to elevated [CO2 ] and temperature for 4 years. A two-component
functional model (Thornley 1970, Amthor 1988) was used to
partition total respiration into growth respiration and maintenance respiration.
and the four walls facing north and east were constructed of a
clear dual-layered acrylic sheet (Standard 16 mm PMMA). A
computer-controlled heat exchanger linked to a refrigeration
unit (CAJ-4511YHR, 3kW, L’Unité-Hermetique, France) was
installed at the top of each chamber.
The computer-controlled heating and cooling system, together with a set of magnetoelectric valves (controlling the
pure CO2 supply), automatically adjusted the temperature and
[CO2 ] inside the chambers to track ambient conditions, or to
achieve a rise in temperature (+ 2 °C during the growing season (April 15 to September 15) and + 6 °C during the off-season (September 16 to April 14)), or a specified enrichment in
[CO2] (+ 350 µmol mol –1 for 24 h day –1 throughout the year),
or both. Further information about the controlled environment
chambers is provided by Kellomäki et al. (2000).
Four treatments were employed: (1) ambient environment
(CON); (2) 2 × ambient [CO2 ] (EC); (3) elevated temperature
(ET); and (4) 2 × ambient [CO2 ] and elevated temperature (EC
+ ET). Each treatment had four replicates.
Needle expansion measurement
One 1-year-old lateral shoot was selected from Whorl 4
branches (counted from the top) facing SE to SW for repeated
measurements of current-year needle expansion and respiration rate. Needles at this stage were considered to be 1 day old
immediately after bud burst, and their area and dry weight
were measured at 72-h intervals throughout the needle expansion period, on the same days on which respiration was measured. Needles that were similar in size and properties to those
used for the respiration measurements were collected and their
areas measured with a scanner and the winNEEDLETM program (Version 4.0, Regent Instruments Inc., Blain, QC, Canada). Needle dry weight was measured after oven drying at
80 °C for 48 h after the area had been measured. Specific
growth rate (SGR; day –1) was calculated as:
Materials and methods
SGR = (lnW2 − lnW1 ) /(t 2 − t1 ),
Site and treatments
The experiment was performed in a naturally seeded stand of
Scots pine near the Mekrijärvi Research Station of the University of Joensuu in Finland (62°47′ N, 30°58′ E, 145 m a.s.l.).
The soil at the site is a sandy loam with a water retention of
40 mm at field capacity and 20 mm at the wilting point for the
top 30 cm of soil. The mean density of the stand is 2500 trees
ha –1. The trees were about 20 years old and had a mean height
of 3.5 m. Further details of the site have been presented by
Kellomäki and Wang (1997).
Sixteen trees of about the same crown size and height were
chosen and individually enclosed in closed-top chambers in
1996. To reduce shading from adjacent trees, all other trees
within 2 m of a chamber were cut down 1 year before the start
of the experiment. The chambers were prismatic, with eight
walls, an internal volume of approximately 26.5 m3 and a
ground area of 5.9 m2. The four walls facing south and west
were constructed of special heating glass with a thin resistance
element converting electricity into heat that is emitted into the
chamber (5640 W for each chamber; Eglars, Ltd., Finland),
(1)
where W is needle dry weight, t is time, and subscripts 1 and 2
represent any 3-day period in the progression of needle expansion.
Measurements of respiration and carbohydrates
Respiration measurements were made between 2200 and
0400 h at 3-day intervals from June to September 2000 with an
ADC gas analyzer (Model LCA-4, Analytic Development
Co., Ltd., U.K.) equipped with a Parkinson cylindrical needle
chamber covered by an opaque cloth. Respiration rates were
determined on four sample needles per treatment. All measurements were made at the [CO2 ] at which the respective
trees were growing. After each measurement, about 3 g of
needles was taken from neighboring shoots and stored at
–80 °C for subsequent carbohydrate analysis (Steen and Larsson 1986).
The temperature coefficient Q10 was measured at temperatures of 5, 10, 15, 20, 25 and 30 °C, proceeding from low to
high temperatures, in June and July. Leaf temperatures were
TREE PHYSIOLOGY VOLUME 21, 2001
ELEVATED CO2 AND TEMPERATURE EFFECTS ON SCOTS PINE
1281
maintained with a temperature controller (Analytic Development Co., Ltd.). The Q10 values measured in June and July
were used to estimate daily total respiration rate for trees in
each treatment.
To determine the effects of elevated [CO2 ] on the growth
and maintenance components of respiration, we regressed specific respiration rate (SRR) against specific growth rate
(Irving and Silsbury 1987, Amthor 1989, Wullschleger and
Norby 1992, Wullschleger et al. 1992a, Sprugel et al. 1995):
(2)
SRR = Rg SGR + Rm ,
where R g (mol CO2 kg –1 dry weight) and Rm (mol CO2 kg –1
day –1) are the growth and maintenance coefficients, respectively, and SRR (mol CO2 kg –1 day –1) is the total integrated
respiration over the 24-h period as determined from instantaneous measurements. Instantaneous rates of respiration in
needles grown in the different environmental treatments were
integrated to daily rates by reference to hourly temperatures
for all the sampling days and the respective mean Q10 values
(Wullschleger et al. 1992a).
Statistical analysis
Analysis of variance (ANOVA) was used to test the effects of
the treatments on needle area, dry weight, carbohydrate concentration and respiration rate. If significant differences were
found, Tukey’s multiple comparisons were used to determine
the difference between treatments.
Treatment effects on the growth and maintenance coefficients of respiration were tested by linear regression and analysis of covariance, and treatment differences in R g and Rm
were determined by standard ANOVA procedures. Covariance analysis assumes similar slopes between the four
treatments in order to test the effects on the intercept. The homogeneity of the slopes between the treatments was tested by
regression analysis before using covariance analysis. The statistical analysis was performed with the SPSS 10.0 software
program (SPSS Science, Chicago, IL).
Figure 1. Area and dry weight of individual Scots pine needles during
the needle expansion period. The trees were grown in four treatments
(CON, EC, ET and EC + ET) for 4 years. Each value is the mean of
four replicates (± SE).
were about 45.1 cm2 g –1 compared with values of 38.7, 52.4
and 50.8 cm2 g –1 for trees in the EC, ET and EC + ET treatments, respectively. The EC treatment reduced SLA by 2–
15% (P = 0.013), whereas the ET and EC + ET treatments increased SLA by 3–16% (P = 0.026) and 1–13% (P = 0.037),
respectively.
Effects of elevated [CO2] and temperature on carbohydrates
During the needle expansion period, the concentrations of
starch, fructose, glucose and sucrose followed similar patterns
in all treatments, although the concentrations varied (Figure 3). Needles exposed to EC had higher soluble sugar and
starch concentrations than CON needles on each sampling
Results
Effects of elevated [CO2] and temperature on growth
During the needle expansion period, dry weight and area of
individual needles followed similar growth patterns in all
treatments (Figure 1). The EC, ET and EC + ET treatments increased needle area and dry weight during the needle expansion period. By the late stage of needle development, the EC,
ET and EC + ET treatments had increased needle area by
about 12, 35 and 33%, respectively, compared with values for
CON trees, and the corresponding increases in needle dry
weight were about 20, 53 and 36%. Overall, the treatments had
significant effects on both needle area and needle dry weight
(P < 0.0005).
In all four treatments, specific leaf area (SLA, cm2 g –1) decreased gradually during needle expansion (Figure 2). In the
late stage of needle development, SLA values for CON trees
Figure 2. Specific needle area as a function of time (days) after bud
burst. The Scots pine trees were grown in four treatments (CON, EC,
ET and EC + ET). Each value is the mean of four replicates.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
1282
ZHA, RYYPPÖ, WANG AND KELLOMÄKI
Figure 3. Concentrations of
starch, glucose, fructose and
sucrose during the needle expansion period in current-year
Scots pine needles. The trees
were grown in four treatments
(CON, EC, ET and EC + ET)
for 4 years. Each value is the
mean of four replicates (± SE).
date, whereas needles in the ET and EC + ET treatments had
lower soluble sugar and starch concentrations than CON needles (Figure 3).
Overall, the treatments had significant effects on carbohydrate concentrations (P = 0.006). The EC treatment significantly increased carbohydrate concentrations (11–23%; P =
0.007) during the needle expansion period, whereas the ET
and EC + ET treatments significantly reduced carbohydrate
concentrations by 7–22% (P = 0.005) and 4–17% (P = 0.004),
respectively. The difference in carbohydrate concentrations
between needles in the ET and EC + ET treatments was not
significant (P = 0.143).
Effects of elevated [CO2] and temperature on respiration
Respiration rates of needles increased exponentially with leaf
temperature in all four treatments (Figure 4). The relationship
could be described by the function:
r = r0 exp( kT ),
(3)
where r0 and k are coefficients specific to the treatment environments (Q10 = exp(10k)). Except for needles in the EC treatment, Q10 values of needles in each treatment were constant
during the growing period (Table 1). Mean Q10 values for the
June and July measurements were 2.09, 2.19, 1.78 and 1.85 for
needles in the CON, EC, ET and EC + ET treatments, respectively. Overall, the EC treatment increased Q10 in the late stage
of needle expansion (P = 0.044), whereas the ET and EC + ET
treatments reduced Q10 (P = 0.031 and 0.042, respectively).
The difference in Q10 between needles in the ET and EC + ET
treatments was not significant (P = 0.127).
Needles in all four treatments exhibited similar trends in
Figure 4. Dark respiration rates of
Scots pine needles as a function of
measurement temperature. The trees
were grown in four treatments (CON,
EC, ET and EC + ET). Measurements
were made in the early (June 29–30)
and late (July 30–31) stages of needle
expansion.
TREE PHYSIOLOGY VOLUME 21, 2001
ELEVATED CO2 AND TEMPERATURE EFFECTS ON SCOTS PINE
Table 1. Effects of four treatments (CON, EC, ET and EC + ET) on
Q10 values calculated from the data in Figure 4. Measurements were
made in the early (June 29–30) and late stages of needle expansion
(July 30–31). Values not followed by a common letter are significantly different from each other at P = 0.05 (ANOVA).
Treatment
CON
EC
ET
EC + ET
Q10
June
July
2.08 ± 0.14 a
2.06 ± 0.19 a
1.76 ± 0.15 a
1.83 ± 0.18 a
2.09 ± 0.17 b
2.32 ± 0.19 c
1.81 ± 0.17 a
1.88 ± 0.14 a
daily respiration rates throughout the needle growing period,
increasing during the early period of needle expansion, reaching their highest values on Day 28 after bud burst, and then
gradually decreasing (Figure 5).
Needle respiration rates of trees in the EC treatment tended
to be higher than those of CON trees up to Day 34 after bud
burst. In the early growing period, EC increased respiration
rates based on dry weight and area by 3–11% (P = 0.071) and
1–9% (P = 0.085), respectively, and reduced them by 5–27%
(P = 0.012) and 2–21% (P = 0.036), respectively, in the late
growing period. The ET and EC + ET treatments increased
needle respiration rates on all sampling dates compared with
needle respiration rates of CON trees. The ET treatment increased needle respiration rates by 12–34% (P < 0.0005) and
1283
8–30% (P < 0.0005) on a dry weight and area basis, respectively, during the needle expansion period. The EC + ET treatment increased needle respiration rates on a dry weight and an
area basis by 10–30% (P < 0.0005) and 5–25% (P < 0.0005),
respectively. Overall, EC significantly reduced needle respiration rates in the late growing period, whereas both ET and
EC + ET significantly increased needle respiration rates.
There was no significant difference between the effects of ET
and EC + ET on needle respiration rates (P = 0.473).
When the two-component functional method was used to
partition needle respiration values into growth and maintenance respiration, SRR proved to be a linear function of SGR
for needles in all four treatments (Figure 6). Although there
was some variation in the growth respiration coefficient (R g
slope) between treatments, it was not statistically significant
(P = 0.214) (Table 2). However, the EC treatment reduced the
maintenance respiration coefficient (R m, y-intercept) by 34%
(P = 0.031), whereas the ET and EC + ET treatments increased
Rm by 29% (P = 0.014) and 21% (P = 0.038), respectively.
Needle respiration rates were closely correlated with specific
growth rate (SGR) in each treatment, with correlation coefficients ranging from 0.95 to 0.98 (Table 2).
Discussion
Effects of elevated [CO2] and temperature on growth
In our study, the EC treatment increased individual needle
Figure 5. Daily total respiration rates
(SRR; mol m –2 day –1 or mol kg –1
day –1) of current-year Scots pine needles during the expansion period. The
trees were grown in four treatments
(CON, EC, ET and EC + ET).
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
1284
ZHA, RYYPPÖ, WANG AND KELLOMÄKI
Figure 6. Relationship between specific respiration rate (SRR) and specific growth rate (SGR) for Scots pine
needles. The trees were grown in four
treatments (CON, EC, ET and EC +
ET). The slope of the regression represents the growth coefficient (mol kg –1)
and the intercept represents the maintenance coefficient (mol kg –1 day –1).
area. Many studies have shown that elevated [CO2 ] increases
total leaf area (Ceulemans and Mousseau 1994, Ceulemans
et al. 1995, Tissue et al. 1997, Saxe et al. 1998, Jach and
Ceulemans 1999, Norby et al. 1999). The increase in total leaf
area in response to elevated [CO2 ] is generally attributed to increases in shoot length and individual needle area. Our finding
that the EC, ET and EC + ET treatments increased individual
needle area by 12, 35 and 33%, respectively (Figure 1), suggests that the treatments resulted in an increase in needle cell
number (Gaudillere and Mousseau 1989) or needle cell expansion rate (Taylor et al. 1993), or both.
The finding that the EC treatment decreased SLA and the
ET and EC + ET treatments increased SLA, reflects the accumulation of carbohydrates in needles of trees in the EC treatment. However, despite the higher SLA in ET- and EC +
ET-treated trees, the ET and EC + ET treatments both increased needle dry weights, presumably because of an ET-induced increase in needle area or needle thickness.
Effects of elevated [CO2] and temperature on carbohydrates
starch, glucose, fructose and sucrose concentrations than
needles exposed to ambient [CO2 ] (Figure 3), which is consistent with previous reports (Barnes et al. 1995, Roberntz and
Stockfors 1998). However, in several studies with conifers, elevated [CO2 ] had no effect on carbohydrate concentrations
(Chomba et al. 1993, Jach and Ceulemans 1999). Carbohydrate accumulation in response to elevated [CO2 ] may indicate
that photosynthate production exceeded demand (Eamus and
Jarvis 1989), or that there were limitations on phloem loading
(Körner et al. 1995).
Carbohydrate concentrations generally decrease in plants
grown under warm conditions (Rowland-Bamford et al.
1996). We observed a decrease in carbohydrate concentrations
in response to the ET treatment (Figure 3). One explanation
for the decrease in concentrations of carbohydrates (starch,
glucose, fructose and sucrose) at high temperatures is that
photosynthetic production is relatively insensitive to temperature, whereas metabolic rates increase with increasing temperature, resulting in increased consumption of assimilates
(Farrar and Williams 1991).
Needles exposed to elevated [CO2 ] had significantly higher
Effects of elevated [CO2] and temperature on respiration
Table 2. Growth (Rg) and maintenance (Rm) coefficients of respiration for current-year needles of Scots pine trees grown in four treatments (CON, EC, ET and EC + ET) for 4 years. The coefficients were
estimated from the regressions shown in Figure 6. Values not followed by a common letter are significantly different from each other
at P = 0.05, according to regression and covariance analyses.
Treatment
Rg (mol kg –1)
Rm (mol kg –1 day –1)
r2
CON
EC
ET
EC + ET
23.04 ± 2.53 a
24.35 ± 3.25 a
25.51 ± 2.66 a
26.77 ± 3.27 a
0.26 ± 0.03 b
0.17 ± 0.03 c
0.37 ± 0.06 a
0.33 ± 0.04 a
0.96
0.97
0.95
0.98
Long-term atmospheric CO2 enrichment slightly increased
needle respiration rates during the early stage of needle expansion, but this effect gradually decreased and by the end of the
needle expansion period EC caused a reduction in respiration
rates (Figure 5), implying a gradual adjustment of the respiratory response to elevated [CO2 ]. Overall, the EC treatment resulted in decreased rates of dark respiration on a needle area or
dry weight basis. This result is partly consistent with previous
observations (Azcón-Bieto and Osmond 1983, Kellomäki and
Wang 1998).
The finding that the EC treatment increased respiration rates
only in the early stage of needle growth suggests that the
long-term effect of EC on dark respiration is mainly indirect.
TREE PHYSIOLOGY VOLUME 21, 2001
ELEVATED CO2 AND TEMPERATURE EFFECTS ON SCOTS PINE
If the reduction in respiration rates were attributable to a
short-term effect, respiration rates would have been reduced
as much in the early growing period as in the late growing period. Our data provided no information about the mechanism(s) underlying the direct and indirect respiratory responses to elevated [CO2 ].
There is much evidence that photosynthesis acclimates to
elevated [CO2 ] in the long term, a process that is accompanied
by increased carbohydrate concentrations (Drake and Gonzàlez-Meler 1997). Based on our observation of a gradual adjustment of the respiratory response to elevated [CO2 ] and the
finding that the EC treatment increased needle carbohydrate
concentrations throughout the needle expansion period, we
postulate that carbohydrates are involved in the acclimation to
[CO2 ] of both respiration and photosynthesis. It is not entirely
clear, however, how carbohydrates modulate respiration or
how carbon is exported from the needles. There may be a positive correlation between carbohydrate concentration and leaf
respiration rate (Thomas and Griffin 1994), or the reduction in
dark respiration in response to EC treatment may be associated
with reduced nocturnal carbon export causing an accumulation of carbohydrates in leaves exposed to CO2-enriched air
(Wullschleger et al. 1992b). Our findings point to a complex
pattern of control exercised by carbohydrates on needle respiration. We did not observe a close relationship between
carbohydrate concentrations and respiration rates. However,
because foliar respiration is unlikely to decrease without a
concomitant decrease in other metabolic processes, it can be
inferred that other biochemical responses will accompany the
decrease in respiratory rate. For example, the decrease in respiration rates of leaves grown at elevated [CO2 ] is accompanied by decreased nitrogen concentrations and a decreased
cost of synthesizing and maintaining leaf proteins (Ryan 1995,
Will and Ceulemans 1997). Reduced N concentrations in response to elevated [CO2 ] have been consistently observed in
Scots pine needles after the expansion period (Kellomäki and
Wang 1998, Jach and Ceulemans 2000, Laitinen et al. 2000),
perhaps indicating that foliage N is involved in the adjustment
of respiration to elevated [CO2 ].
Elevated temperature alone or together with elevated [CO2 ]
significantly increased needle respiration rates. Long-term elevated temperature enhances the activities of many enzymes,
thus increasing the rates of enzyme-catalyzed synthetic processes in sink needles and thereby increasing sink metabolic
rates, which will result in increased sink strength, assimilate
transport and respiratory rates. Because increased rates of respiration and assimilate utilization will minimize or prevent the
accumulation of carbohydrates in source leaves, a similar explanation could account for the reduction in needle carbohydrate concentrations in response to long-term exposure to ET
or ET + EC (Farrar and Williams 1991). This explanation
could also partly account for the increase in the maintenance
component of respiration caused by the ET and EC + ET treatments.
The EC, ET and EC + ET treatments had no significant effect on the growth respiration coefficient of needles. In contrast, EC treatment reduced the maintenance respiration coef-
1285
ficient, indicating that the reduction in respiration in response
to elevated [CO2 ] was mainly attributable to the maintenance
component. The finding that both the ET and EC + ET treatments significantly increased the maintenance respiration coefficient indicates that the maintenance respiration coefficient
is more sensitive to temperature than the growth respiration
coefficient. This implies that long-term warming is likely to
affect the balance between growth and respiration (cf. Ryan
1991). We postulate that the increase in the maintenance respiration coefficient in response to ET treatment is related to increased enzyme activities in the respiratory process brought
about by elevated temperature. Furthermore, we suggest that
long-term elevated temperature stimulates sink metabolism or
accelerates phloem loading of needles, or both, causing a reduction in needle carbohydrate concentrations.
When growth and maintenance costs were estimated over
the 67-day growing period (Table 3), EC reduced maintenance
costs by 34% compared with the CON treatment, but ET and
EC + ET increased maintenance costs by 29 and 21%, respectively. The relative contribution of the maintenance component to total needle respiration was 16, 26 and 23% in trees in
the EC, ET and EC + ET treatments, respectively, compared
with 23% in trees in the CON treatment.
Although the Q10 values of trees in the various treatments
remained relatively constant during needle expansion, they
varied from one treatment to another. The low Q10 recorded in
ET-treated trees could reduce carbon loss caused by high temperature. The lower Q10 in trees in the ET and EC + ET treatments than in the CON treatment may imply that downward
temperature acclimation occurred. Downward acclimation of
respiration to elevated temperature has been commonly observed, although the degree of acclimation varies with species
(Tjoelker et al. 1999).
A positive correlation between specific growth rate and specific respiration rate has been observed (Azcón-Bieto et al.
1983, Amthor 1989, Poorter et al. 1990). Because the rate of
leaf growth has a large impact on leaf respiration, respiration
rates of expanding leaves at varying growth stages must be
taken into account when estimating whole-tree carbon dynamics and when modeling the respiratory response to elevated
[CO2 ].
In summary, elevated [CO2 ] and temperature increased both
needle area and needle dry weight. However, some effects of
Table 3. Estimates of the growth and maintenance costs over a 67-day
growing period of current-year needles of Scots pine trees grown in
four treatments (CON, EC, ET and EC + ET). Estimates were based
on Equation 2. Within a treatment, values in parentheses indicate the
percent contribution of growth and maintenance respiration to total
respiration of needles.
Respiration costs
(g g –1 season –1)
CON
EC
ET
EC + ET
Growth
Maintenance
Total
2.53 (77)
0.76 (23)
3.29
2.75 (84)
0.50 (16)
3.25
3.09 (74)
1.09 (26)
4.18
3.18 (77)
0.97 (23)
4.15
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
1286
ZHA, RYYPPÖ, WANG AND KELLOMÄKI
elevated [CO2 ] and temperature were antagonistic. Elevated
[CO2 ] increased needle carbohydrate concentrations and decreased needle respiration rates after the needle expansion
period, whereas elevated temperatures decreased needle carbohydrate concentrations and increased needle respiration
rates. Neither elevated [CO2 ] nor elevated temperature, either
separately or together, had any significant effect on the growth
respiration coefficient, but elevated temperature both alone
and in combination with elevated [CO2 ] significantly increased the maintenance respiration coefficient. Because
changes in dark respiration of needles developed under conditions of elevated [CO2 ] and temperature may involve many
physiological and biochemical processes, and also morphological changes, these processes need to be considered when
interpreting respiratory response to changes in [CO2 ] and temperature. Our measurements of respiration were restricted to
current-year needles at a specific position in the canopy, but to
estimate whole-canopy respiration and its response to elevated
[CO2 ] and temperature it will be necessary to consider the effects of needle age and canopy position as well.
Acknowledgments
This work was funded through the Finnish Centre of Excellence
Programme (2000–2005) under the Centre of Excellence for Forest
Ecology and Management (Project No. 64308), coordinated by Prof.
Seppo Kellomäki, University of Joensuu, Faculty of Forestry. In this
context, funding provided by the Academy of Finland, the National
Technology Agency (Tekes) and the University of Joensuu is gratefully acknowledged. We thank Matti Lemettinen for taking care of the
experiment at the Mekrijärvi Research Station, and Maini Mononen
for help in the laboratory.
References
Amthor, J.S. 1988. Growth and maintenance respiration in leaves of
bean (Phaseolus vulgaris L.) exposed to ozone in open-top chambers in the field. New Phytol. 110:319–325.
Amthor, J.S. 1989. Respiration and crop productivity. SpringerVerlag, New York, 215 p.
Amthor, J.S. 1991. Respiration in a future, higher CO2 world. Plant
Cell Environ. 14:13–20.
Amthor, J.S. 2000. Direct effect of elevated CO2 on nocturnal in situ
leaf respiration in nine temperate deciduous tree species is small.
Tree Physiol. 20:139–144.
Arnone, J.A. and C. Körner. 1997. Temperature adaptation and acclimation potential of leaf dark respiration in two species of Ranunculus from warm and cold habitats. Arct. Alp. Res. 29:122–125.
Atkin, O.K., C. Holly and M.C. Ball. 2000. Acclimation of snow gum
(Eucalyptus pauciflora) leaf respiration to seasonal and diurnal
variations in temperature: the importance of changes in the capacity and temperature sensitivity of respiration. Plant Cell Environ.
23:15–26.
Azcón-Bieto, J. 1992. Relationships between photosynthesis and
respiration in the dark in plants. In Trends in Photosynthesis Research. Eds. J. Barber, M.G. Guerrero and H. Medrano. Intercept,
Andover, Hampshire, U.K., pp 241–253.
Azcón-Bieto, J. and C.B. Osmond. 1983. Relationship between photosynthesis and respiration. Plant Physiol. 98:757–760.
Azcón-Bieto, J., H. Lamber and D.A. Day. 1983. Effect of photosynthesis and carbohydrate status and involvement of the alternative
pathway in leaf respiration. Plant Physiol. 72:598–603.
Baker, J.T., F. Laugel, K.J. Boote and J.L.H. Allen. 1992. Effects of
daytime carbon dioxide concentration on dark respiration in rice.
Plant Cell Environ. 15:231–239.
Barnes, J.D., T. Pfirmann, K. Steiner, C. Lütz, U. Busch, H. Küchenhoff and H.D. Payer. 1995. Effects of elevated CO2, elevated O3
and potassium deficiency on Norway spruce (Picea abies (L.)
Karst.): seasonal changes in photosynthesis and non-structural carbohydrate content. Plant Cell Environ. 18:1345–1357.
Bunce, J.A. and F. Caulfield. 1991. Reduced respiratory carbon dioxide efflux during growth at elevated carbon dioxide in three herbaceous perennial species. Ann. Bot. 67:325–330.
Ceulemans, R. and M. Mousseau. 1994. Effects of elevated atmospheric CO2 on woody plants. New Phytol. 127:425–446.
Ceulemans, R., I.A. Janssens and M.E. Jach. 1999. Effects of CO2 enrichment on trees and forests: lessons to be learned in view of future ecosystem studies. Ann. Bot. 84:577–590.
Ceulemans, R., X.N. Jang and B.Y. Shao. 1995. Growth and physiology of one-year old poplar (Populus) under elevated atmospheric
CO2 levels. Ann. Bot. 75:609–617.
Chomba, B.M., R.D. Guy and H.G. Weger. 1993. Carbohydrate reserve accumulation and depletion in Engelmann spruce (Picea
engelmannii Parry): effects of cold storage and prestorage CO2 enrichment. Tree Physiol. 13:351–364.
Curtis, P.S., C.S. Vogel, K.S. Pregitzer, D.R. Zak and J.A. Teeri.
1995. Interacting effects of soil fertility and atmospheric CO2 on
leaf area growth and carbon gain physiology in Populus ×
euramericana (Dode) Guinier. New Phytol. 129:253–263.
Drake B.G. and M.A. Gonzàlez-Meler. 1997. More efficient plants: a
consequence of rising atmospheric CO2? Plant Mol. Biol. 48:
609–639.
Drake, B.G. 1992. The impact of rising CO2 on ecosystem production. Water Air Soil Pollut. 64:25–44.
Eamus, D. and P.G. Jarvis. 1989. The direct effect of increase in the
global atmospheric CO2 concentration on natural and commercial
temperate trees and forests. In Advances in Ecological Research.
Eds. M. Begon, A. H. Fitter, E.D. Ford and A. Macfayden. Academic Press, New York, pp 1–41.
Farrar, J.F. and M.L. Williams. 1991. The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning,
source–sink relations and respiration. Plant Cell Environ. 14:
819–830.
Gaudillere, J.P. and M. Mousseau. 1989. Short term effect of CO2 enrichment on leaf development and gas exchange of young poplars
(Populus euramericana cv I 214). Oecologia 95:575–580.
Gifford, R.M., H. Lambers and J.I.L. Morison. 1985. Respiration of
crop species under CO2 enrichment. Physiol. Plant. 63:351–356.
Griffin, K.L., J.T. Ball and B.R. Strain. 1996. Direct and indirect effects of elevated CO2 on whole-shoot respiration in ponderosa pine
seedlings. Tree Physiol. 16:33–41.
Gunderson, C.A., R.J. Norby and S.D. Wullschleger. 2000. Acclimation of photosynthesis and respiration to simulated climatic warming in northern and southern populations of Acer saccharum: laboratory and field evidence. Tree Physiol. 20:87–96.
Hrubec, T.C., J.M. Robinson and R.P. Donaldson. 1985. Effects of
CO2 enrichment and carbohydrate content on the dark respiration
of soybeans. Plant Physiol. 79:684–689.
Irving, D.E. and J.H. Silsbury. 1987. A comparison of the rate of
maintenance respiration in some crop legumes and tobacco determined by three methods. Ann. Bot. 59:257–264.
Jach, M.E. and R. Ceulemans. 1999. Effects of elevated atmospheric
CO2 on phenology, growth and crown structure of Scots pine
(Pinus sylvestris) seedlings after two years of exposure in the field.
Tree Physiol. 19:289–300.
TREE PHYSIOLOGY VOLUME 21, 2001
ELEVATED CO2 AND TEMPERATURE EFFECTS ON SCOTS PINE
Jach, M.E. and R. Ceulemans. 2000. Short- versus long-term effects
of elevated CO2 on night-time respiration of needles of Scots pine
(Pinus sylvestris L.). Photosynthetica 38:57–67.
Jarvis, P.G. 1998. Effects of climate change on ecosystem carbon balance. In Earth’s Changing Land, GCTE–LUCC Open Science
Conference on Global Change Abstracts. Institute Cartografic de
Catalunya, Barcelona, 198 p.
Kellomäki, S. and K.Y. Wang. 1997. Effects of elevated O3 and CO2
concentrations on phtosynthesis and stomatal conductance in Scots
pine. Plant Cell Environ. 20:995–1006.
Kellomäki, S. and K.Y. Wang. 1998. Growth, respiration and nitrogen content in needles of Scots pine exposed to elevated ozone and
carbon dioxide in the field. Environ. Pollut. 101:263–274.
Kellomäki, S., K.Y. Wang and M. Lemettinen. 2000. Controlled environment chambers for investigating tree response to elevated CO2
and temperature under boreal conditions. Photosynthetica 38:
69–81.
Körner, C., S. Pelaen-Riedl and A.J.E. Van Bel. 1995. CO2 responsiveness of plants: a positive link to phloem loading. Plant Cell
Environ. 18:595–600.
Kozlowski, T.T., P.J. Kramer and S.G. Pallardy. 1991. The physiological ecology of woody plants. Academic Press, New York,
796 p.
Laitinen, K., E.M. Luomala, S. Kellomäki and E. Vapaavuori. 2000.
Carbon assimilation and nitrogen in needles of fertilized and unfertilized field-grown Scots pine at natural and elevated concentration
of CO2. Tree Physiol. 20:881–892.
Mousseau, M. and B. Saugier. 1992. The direct effect of increased
CO2 on gas exchange and growth of forest tree species. J. Exp. Bot.
43:1121–1130.
Nijs, I., I. Impens and T. Behaeghe. 1989. Leaf and canopy responses
of Lolium perenne to long-term elevated atmospheric carbon dioxide concentration. Planta 177:312–320.
Norby, R.J., S.D. Wullschleger, C.A. Gunderson, D.W. Johnson and
R. Ceulemans. 1999. Tree responses to rising CO2 in field experiments: implications for the future forest. Plant Cell Environ. 22:
683–714.
Poorter, H., C. Remkes and H. Lambers. 1990. Carbon and nitrogen
economy of 24 wild species differing in relative growth rate. Plant
Physiol. 94:621–627.
Reuveni, J. and J. Gale. 1985. The effect of high levels of carbon dioxide on dark respiration and growth of plants. Plant Cell Environ.
8:623–628.
Roberntz, P. and J. Stockfors. 1998. Effects of elevated CO2 concentration and nutrition on net photosynthesis, stomatal conductance
and needle respiration of field-grown Norway spruce trees. Tree
Physiol. 18:233–241.
Rowland-Bamford, A.J., S.J. Baker, L.H. Allen and G. Bowes. 1996.
Interactions of CO2 enrichment and temperature on carbohydrate
accumulation and partitioning in rice. Environ. Exp. Bot. 36:
111–124.
Ryan, M.G. 1991. Effects of climate change on plant respiration.
Ecol. Appl. 1:157–167.
1287
Ryan, M.G. 1995. Foliar maintenance respiration of subpine and boreal trees and shrubs in relation to nitrogen content. Plant Cell Environ. 18:765–772.
Ryan, M.G., M.B. Lavigne and S.T. Gower. 1997. Annual carbon
cost of autotropic respiration in boreal forest ecosystems in relation
to species and climate. J. Geophys. Res. 102:28,871–28,883.
Saxe, H., D.S. Ellsworth and J. Heath. 1998. Tree and forest functioning in an enriched CO2 atmosphere. New Phytol. 139:395–436.
Sprugel, D.G., M.G. Ryan, J.R. Brooks, K.A. Vogt and T.A. Martin.
1995. Respiration from the organ level to the stand. In Resource
Physiology of Conifers. Eds. W.K. Smith and T.M. Hinckley. Academic Press, San Diego, pp 255–299.
Steen, E. and K. Larsson. 1986. Carbohydrates in roots and rhizomes
of perennial grasses. New Phytol. 104:339–346.
Taylor, G., S.D.L. Gardner, C. Bosac and T.J. Flowers. 1993. Influence of elevated CO2 on the water relations and biophysics of cell
growth of farm woodland trees. J. Environ. Bot. 44(Suppl.):12.
Teskey, R.O. 1995. A field study of the effects of elevated CO2 on
carbon assimilation, stomatal conductance and leaf and branch
growth of Pinus taeda trees. Plant Cell Environ. 18:565–573.
Thomas, R.B. and K.L. Griffin. 1994. Direct and indirect effects of atmospheric carbon dioxide enrichment on leaf respiration of
Glycine max (L.) Merr. Plant Physiol. 104:355–361.
Thornley, J.H.M. 1970. Respiration, growth and maintenance in
plants. Nature 227:304–305.
Tissue, D.T., R.B. Thomas and B.R. Strain. 1997. Atmospheric CO2
enrichment increases the growth and photosynthesis in Pinus
taeda: a 4-year experiment in the field. Plant Cell Environ. 20:
1123–1134.
Tjoelker, M.G., J. Oleksyn and P.B. Reich. 1999. Acclimation of respiration to temperature and CO2 in seedlings of boreal tree species
in relation to plant size and relative growth rate. Global Change
Biol. 5:679–691.
Will, R. 2000. Effects of different day-time and night-time temperature regimes on the foliar respiration of Pinus taeda: predicting the
effect of variable temperature on acclimation. J. Exp. Bot. 51:
1733–1739.
Will, R.E. and R. Ceulemans. 1997. Effects of elevated CO2 concentration on photosynthesis, respiration and carbohydrate status of
coppice Populus hybrids. Physiol. Plant. 100:933–939.
Wullschleger, S.D. and R.J. Norby. 1992. Respiratory cost of leaf
growth and maintenance in white oak saplings exposed to atmospheric CO2 enrichment. Can. J. For. Res. 22:1717–1721.
Wullschleger, S.D., L.H. Ziska and J.A. Bunce. 1994. Respiratory responses of higher plants to atmospheric CO2 enrichment. Physiol.
Plant. 90:221–229.
Wullschleger, S.D., R.J. Norby and C.A. Gunderson. 1992a. Growth
and maintenance respiration in leaves of Liriodendron tulipifera L.
exposed to long-term carbon dioxide enrichment in the field. New
Phytol. 121:515–523.
Wullschleger, S.D., R.J. Norby and D.L. Hendrix. 1992b. Carbon exchange rates, chlorophyll content, and carbohydrate status of two
forest tree species exposed to carbon dioxide enrichment. Tree
Physiol. 10:21–31.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com