Tree Physiology 22, 41–49
© 2002 Heron Publishing—Victoria, Canada
Influence of tree internal nitrogen reserves on the response of beech
(Fagus sylvatica) trees to elevated atmospheric carbon dioxide
concentration
JENS DYCKMANS1,2 and HEINER FLESSA1
1
Institute of Soil Science and Forest Nutrition, University of Göttingen, Büsgenweg 2, 37077 Göttingen, Germany
2
Author to whom correspondence should be addressed ([email protected])
Received May 16, 2001; accepted July 14, 2001; published online December 1, 2001
Summary We examined the influence of plant internal nitrogen (N) reserves on the response of 3-year-old beech (Fagus
sylvatica L.) trees to elevated atmospheric CO2 concentration
([CO2 ]) in a dual 15N and 13C long-term labeling experiment.
Trees were grown on sand and received either no N nutrition
(–N treatment) or 4 mM N (+N treatment) for 1 year. The –N
and +N pretreated trees were then placed in growth chambers
and grown in 350 (ambient) or 700 ppm (elevated) of a 13CO2
atmosphere for 24 weeks. In all treatments, trees were supplied
with 4 mM 15N during the experiment.
Irrespective of tree N reserves, elevated [CO2 ] increased cumulative carbon (C) uptake by about 30% at Week 24 compared with that for trees in the ambient treatment. Elevated
[CO2 ] also caused a shift in C allocation to belowground compartments, which was more pronounced in –N trees than in +N
trees. In +N trees, belowground allocation of new C at
Week 24 was 67% in ambient [CO2 ] compared with 70% in elevated [CO2 ]. The corresponding values for –N trees were 70
and 79%. The increase in C allocation in response to elevated
[CO2 ] was most evident as an increase in belowground respiration; however, specific root respiration was unaffected by
the CO2 or N treatments.
Although elevated [CO2 ] increased root growth and belowground respiration, it had no effect on N uptake at Week 24.
As a result of increased C uptake, N concentrations were decreased in trees in the elevated [CO2 ] treatment compared with
trees in the ambient treatment in both N treatments. Partitioning of new N uptake was unaffected by elevated [CO2 ] in
+N trees. In –N trees, however, N allocation to the stem decreased in response to elevated [CO2 ] and N allocation to fine
roots increased, suggesting a reduction in the formation of N
reserves in response to elevated [CO2 ]. We conclude that the
response of beech trees to elevated [CO2 ] is affected by internal N status and that elevated [CO2 ] may influence the ability
of the trees to form N reserves.
Keywords: carbon uptake, nitrogen storage, nitrogen uptake,
partitioning, root respiration, stable isotope.
Introduction
Increases in atmospheric carbon dioxide concentration ([CO2 ])
are likely to result in increased carbon (C) uptake by most tree
species (Curtis 1996, Saxe et al. 1998), including beech
(Fagus sylvatica L.) (Overdieck and Forstreuter 1995, Heath
and Kerstiens 1997, Dyckmans et al. 2000a). There is also evidence that elevated [CO2 ] decreases tissue nutrient concentrations (McGuire et al. 1995, Peñuelas and Estiarte 1997). This
might be a dilution effect caused by increased carbon uptake;
however, it could be a result of increased nitrogen-use efficiency (Arp et al. 1998, Centritto and Jarvis 1999). Soil nitrogen (N) availability is one of the main factors limiting growth
in forest ecosystems (Cole 1981). There have been numerous
studies on the effect of soil N availability on C assimilation
and N uptake (El Kohen and Mousseau 1994, Ericsson et al.
1996, Tissue et al. 1997, Bucher et al. 1998, Maillard et al.
2001). The availability of external N also has considerable influence on the response of trees to elevated atmospheric [CO2 ]
(Saugier 1998). Low soil N availability may substantially reduce potential growth rate at elevated [CO2 ] and thus limit the
long-term growth response to elevated [CO2 ] (Saxe et al.
1998, Murray et al. 2000). However, in trees (especially deciduous species), growth depends not only on an external N supply but also on internal N reserves (Dickson 1989, Millard
1996). The ecological significance of N storage is that it uncouples growth from N uptake and allows growth to occur
when external N availability is low (Chapin et al. 1990). In
beech, growth is strongly determined by internal N reserves
(Dyckmans and Flessa 2001). However, there is no information on the effect of the internal N status of beech trees on
growth in elevated [CO2 ].
Atmospheric [CO2 ] and tree internal N status not only affect
total growth rate, but may also alter allocation patterns of C
and N and thereby strongly influence the long-term response
of trees to environmental changes. Although information on C
and N allocation in different tree species under changing environmental conditions is widely available (Burke et al. 1992,
Canham et al. 1996), there are few quantitative data on allocation patterns and their temporal changes. Carbon allocation to
42
DYCKMANS AND FLESSA
roots and root respiration are key processes, but little is known
about their responses to elevated [CO2 ] (Hendrick and Pregitzer 1993, Horwath et al. 1994), because most studies have focused on the aboveground effects of elevated [CO2 ] (Saxe et
al. 1998).
The objectives of our study on young beeches were to: (1)
quantify the impact of elevated [CO2 ] on the uptake of C and
N; (2) assess the effect of elevated [CO2 ] on the patterns of C
and N translocation; and (3) determine the influence of internal N reserves on the response of beech trees to elevated
[CO2 ]. Because determination of the partitioning of newly acquired C and N in different plant compartments requires techniques that differentiate between external and internal nutrient
sources, we designed a continuous dual 13C and 15N labeling
experiment (Deléens et al. 1983, Vivin and Guehl 1997, Dyckmans et al. 2000b) to investigate the study objectives.
Materials and methods
Plant material and treatments
Three-year-old nursery-grown beech trees (Fagus sylvatica)
were examined. Pretreatments were applied to produce trees
differing in internal N status. Half the study trees were
supplied with unlabeled N in the year before the experiment
(+N treatment), whereas the remaining trees received no N in
the year before the experiment (–N treatment). At the end of
the 1-year pretreatment period, the N concentration of the –N
trees was 0.58% compared with 0.85% for the +N trees,
although the dry matter of trees did not differ significantly between N treatments (see Table 1).
For the CO2 experiment, the +N and –N trees were each divided into two groups and assigned to the 350 and 700 ppm
13
CO2 treatments in a full factorial design (+N + 350 ppm CO2
(+N;350); +N + 700 ppm CO2 (+N;700); –N + 350 ppm CO2
(–N;350); and –N + 700 ppm CO2 (–N;700)). All trees in both
CO2 treatments received 4 mM N fertilizer as 2 mM
15
NH 415NO3 during the CO2 experiment. For all treatments,
trees were placed in the growth chambers approximately
3 weeks before bud break. Bud break was defined as the week
(Week = 0) when the first green leaves became visible.
Griesheim, Duisburg, Germany) to maintain 350 and 700 ppm
CO2 in the ambient and elevated [CO2 ] treatments, respectively. The chambers provided a 12-h photoperiod at a photosynthetic photon flux density of 130 µmol m –2 s –1. Day/night
temperature was 18/13 °C, and relative humidity was maintained at 75%. Details of the growth chamber system are given
in Dyckmans et al. (2000a, 2000b).
Plant sampling and analysis
At the beginning of the experiment (Week 0; corresponding
with time of bud break for trees in all treatments) and after 6,
12, 18 and 24 weeks of exposure to the CO2 treatments, five
plants per treatment were harvested. The plants were divided
into buds, leaves, branches, stem, coarse roots (< 2 mm) and
fine roots (> 2 mm). Plant samples were dried at 65 °C and
finely ground.
Total C and N contents and 13C/12C and 15N/14N isotope ratios were determined with an isotope ratio mass spectrometer
(IRMS Deltaplus, Thermo Finnigan Mat, Bremen, Germany)
coupled to an elemental analyzer (EA 1108, Fisons, Rodano,
Milan, Italy) in online mode.
Belowground respiration
Because the plants were grown on carbon-free sand, CO2
efflux from the root compartment was exclusively root-derived and represented the sum of root respiration and microbial and fungal respiration of root-derived organic carbon, and
is referred to hereafter as belowground respiration. It was determined weekly by taking gas samples from the root compartments before the end of the night, which were stored in sealed
vials. The CO2 concentration and isotopic ratio (13C/12C) were
measured with a continuous flow GC-IRMS system (Delta C,
Thermo Finnigan Mat) and the belowground respiration calculated.
Specific belowground respiration was calculated from belowground respiration shortly before harvesting, divided by
the amount of new C in the fine root fraction at harvest (i.e., at
Weeks 6, 12, 18 and 24). We used specific belowground respiration as a measure of new fine root activity.
Calculation of C and N allocation
Microcosms and growth chamber
For the CO2 experiment, the +N and –N trees were planted in
sand in PVC cylinders (height 0.3 m, diameter 0.14 m) and the
soil compartment was separated from the aboveground atmosphere by sealing the opening around each tree with a plastic
stopper and solvent-free putty. The headspace of about
800 cm3 in each soil compartment was continuously flushed
with CO2-free air at a rate of 0.17 cm3 s –1. Irrigation was
achieved by weekly feeding of 130 cm3 of a Hoagland-based
nutrient solution (2 mM 15NH 415NO3, 25 atom% 15N) applied
with a syringe. The microcosms were installed in growth
chambers into which CO2-free air was continuously supplied
at a rate of 125 cm3 s –1. A CO2 analyzer (UNOR 610, Maihak,
Hamburg, Germany) connected to the growth chamber controlled the injection of CO2 with δ13C = –48.0‰ (Messer-
The labeling of the chamber atmosphere and the N fertilizer
facilitated differentiation between the uptake of C and N during the experiment and C and N in the preexisting plant material. Hereafter, the C and N taken up by the trees during the
experiment is referred to as new C and new N, respectively.
The isotopic signal for C was expressed as δ13C:
δ13C =
Rsample
1000,
Rstandard − 1
(1)
where R is the 13C/12C ratio and Pee Dee Belemnite is the standard.
The isotopic signal for N was expressed as an absolute proportion (A%) and was derived as:
TREE PHYSIOLOGY VOLUME 22, 2002
INFLUENCE OF N STORES ON THE REACTION OF BEECH TO ELEVATED [CO2]
43
Table 1. Effects of CO2 and N treatments on dry matter (DM), N concentration, relative specific allocation (RSA) of C and N, belowground C release and aboveground partitioning of new C and new N at Weeks 0 and 24. Values are means with standard deviation in parentheses (n = 5).
Treatment
DM (g)
+N
–N
N (%)
+N
–N
RSA new C (%)
+N
–N
RSA new N (%)
+N
–N
Cumulative belowground respiration (g C tree –1)
+N
–N
Aboveground partitioning of new C (%)
+N
–N
Aboveground partitioning of new N (%)
+N
–N
A% =
15
14
N
100.
N + 15 N
(2)
Relative specific allocation (RSA) describes the fraction of
newly incorporated C or N in the tissue ( fnew) relative to total C
or N in a given sample (Deléens et al. 1994). The RSA was calculated from:
E p = f new E1 + (1 − f new) E c ,
f new =
E p − Ec
E1 − Ec
= RSA (newE),
(3)
(4)
where Ep is the isotopic signal (i.e., δ13C for C or A% for N) of
the plant sample, E c is isotopic signal of the unlabeled control
plants and El is isotopic signal of 15N in the nutrient solution or
of 13C in the plant. The isotopic signal of 13C in the plant was
influenced by the isotopic signal of the air supply and the discrimination during plant uptake. Assuming that new root tips
consisted exclusively of new assimilates, the isotopic signals
of root tips harvested at Week 12 were used as a standard for El
(Dyckmans et al. 2000a). This approach accounts for both the
13
C labeling of the chamber atmosphere and the 13C discrimination during C assimilation in the 350 and the 700 ppm treat-
350 ppm CO2
700 ppm CO2
Week 0
Week 24
Week 0
Week 24
17.1
(6.1)
19.3
(5.5)
0.85
(0.17)
0.58
(0.05)
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
29.0
(3.1)
23.3
(0.9)
0.82
(0.04)
0.98
(0.07)
36.1
(2.8)
33.5
(5.2)
27.5
(1.9)
43.0
(3.8)
2.15
(0.35)
1.58
(0.19)
33.2
(2.3)
30.2
(2.0)
37.7
(18.4)
47.1
(2.0)
17.1
(6.1)
19.3
(5.5)
0.85
(0.17)
0.58
(0.05)
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
28.4
(2.4)
26.0
(4.2)
0.80
(0.04)
0.91
(0.10)
45.6
(6.0)
36.8
(5.4)
27.7
(5.5)
40.7
(2.3)
2.76
(0.46)
2.69
(0.72)
29.5
(5.5)
20.7
(2.6)
49.9
(13.6)
33.4
(6.3)
ment, respectively.
Partitioning (%P) describes the proportion of newly acquired (labeled) element in a given plant organ relative to the
total labeled element in the whole plant (Deléens et al. 1994).
Partitioning of the new C and new N was calculated as:
% PE =
Eorgan f new
E plant f new
organ
100,
(5)
plant
where Eorgan is amount of new C or new N in the specific plant
organ and Eplant is the amount of new C (including belowground respiration) or new N in the whole plant.
Statistical analysis
The results were expressed as arithmetic means with standard
deviation. The significance of treatment effects was tested by
analysis of variance (ANOVA). Treatment effects on C and N
uptake and partitioning at the whole-plant level and in different plant organs were analyzed by three-way ANOVA
(growth duration, atmospheric [CO2 ], internal N status; repeated measurement design; n = 5). Probabilities of less than
0.05 were considered to be significant and probabilities of
0.1 > P ≥ 0.05 were considered to indicate a trend.
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44
DYCKMANS AND FLESSA
Figure 1. Effects of the CO2 and N treatments on total amount of new
C taken up by the trees (including belowground respiration) 6, 12 and
24 weeks after bud break. Means and standard deviation (n = 5).
Results
Carbon uptake and partitioning of new C
Uptake of new C was markedly affected by elevated [CO2 ]
and amount of internal N reserves (Figure 1). Increased C uptake in response to elevated [CO2 ] and decreased C uptake in
response to reduced N reserves was observed as early as
Week 6 (6 weeks after bud break) and persisted for the whole
season. At Week 6, total uptake of new C ranged between
0.8 (–N;350 treatment) and 1.8 g (+N;700 treatment, Figure 1). At the end of the experiment (Week 24), these values
were 4.2 g in the –N;350 treatment and 7.7 g in the +N;700
treatment, resulting in RSA of new C of 33.5 and 45.6%, respectively (Table 1). At Week 24 in elevated [CO2 ], there was
a 30% increase in C uptake in both +N and –N trees (Figure 1)
and C uptake was about 40% higher for +N trees than for –N
trees (Figure 1). The effect of reduced internal N reserves on C
uptake was paralleled by a decrease in total tree biomass (Tables 1 and 2). There was a trend toward increased dry matter in
the [CO2 ] treatment (Tables 1 and 2).
Partitioning of new C showed a distinct seasonal pattern
(Figure 2): at Week 6, leaves were the main C sink (between
35 and 40% of all new carbon was allocated there). Subsequently, allocation shifted and at Week 24 more than 55% of
the total new C was accounted for by fine roots and belowground respiration in all treatments (Figure 2). Partitioning of
new C was affected by elevated [CO2 ] in both +N and –N
trees. However, the effects were more pronounced in –N trees
than in +N trees. Elevated [CO2 ] resulted in a shift in C allocation to fine roots (Figure 2, Table 2) and belowground respiration was increased by 29% in +N trees and 70% in –N trees
(Table 1). The large increase in belowground allocation was
accompanied by a decline in partitioning to the stem in the
–N;700 treatment (7.3% at Week 24) compared with the other
three treatments (13–16% at Week 24, Figure 2b).
Belowground respiration was between 5 and 8 mg C day –1
for all treatments before bud break and increased markedly
soon after bud break (Figure 3a). Maximum values of 26 mg C
day –1 for the +N;350 treatment and 13 mg C day –1 for the
–N;350 treatment (Figure 3a) were reached at about Week 12.
Toward the end of the experiment, belowground respiration
decreased slightly in all treatments. Elevated [CO2 ] caused an
increase in belowground respiration and the increase was
more pronounced in the –N treatments than in the +N treatments. The RSA of new C in belowground respiration increased considerably after bud break in all treatments and the
majority of the respired carbon (> 80%) originated from uptake of C after Week 6 (Figure 3b). The RSA of new C was
higher in trees in elevated [CO2 ] than in trees in ambient [CO2 ]
but was unaffected by N treatment.
Specific belowground respiration was highest at Week 6
and then decreased throughout the rest of the growing season
(Figure 4), mainly because of a corresponding increase in new
fine root biomass. Except for Week 6, when specific belowground respiration was substantially higher in the –N treatment compared with the +N treatment, no effects of [CO2 ] and
N nutrition were observed. At Week 24, specific belowground
respiration was about 10 mg C day –1 (g Cnew, fineroots) –1 for all
treatments.
Table 2. Three-factorial analysis of variance (ANOVA) for dry matter (DM), N concentration ([N]), N content, new C content (C new), RSA of
new C (RSAC) and RSA of new N (RSAN), aboveground partitioning of new C and new N, partitioning of new C and new N to fine roots and cumulative belowground respiration (CBR) at Weeks 6–24 (n = 5). Significance: ns = not significant; ° = P < 0.1; * = P < 0.05; ** = P < 0.01; and
*** = P < 0.005.
Factors
Growth duration (G)
N nutrition (N)
[CO2 ]
G×N
G × [CO2 ]
N × [CO2 ]
G × N × [CO2 ]
Error
P-Value
DM
[N]
(%)
N
(g)
C new RSA C
(g)
RSAN
New C
New N
New C
above ground above ground fine roots
New N
fine roots
CBR
(g tree –1)
***
***
°
ns
ns
ns
ns
2.6%
***
ns
°
***
ns
ns
ns
3.0%
***
***
ns
**
*
ns
ns
1.8%
***
***
***
ns
ns
ns
ns
0.8%
***
***
ns
°
ns
ns
ns
0.3%
***
***
***
ns
ns
ns
ns
0.8%
**
***
ns
**
ns
***
ns
2.2%
***
**
***
ns
**
ns
ns
0.7%
***
***
***
ns
ns
ns
ns
0.7%
**
ns
ns
°
ns
***
ns
3.6%
TREE PHYSIOLOGY VOLUME 22, 2002
***
°
**
ns
ns
ns
ns
3.0%
INFLUENCE OF N STORES ON THE REACTION OF BEECH TO ELEVATED [CO2]
45
content between the –N and +N trees decreased during the
CO2 experiment, and at Week 24, mean N content was 0.23 ±
0.01 g tree –1 for all treatments. Elevated [CO2 ] had no effect
on tree N content at any time. Reflecting the reduced C uptake
by –N trees, N concentrations were greater in –N trees than in
+N trees during the second half of the growing season (Table 1). The RSA of new N was higher in –N trees than in +N
trees on all sampling dates. This was mainly because the –N
trees had reduced N reserves; it does not indicate higher N uptake by –N trees during the experiment. Elevated [CO2 ] had no
effect on the RSA of new N (Tables 1 and 2), indicating the N
uptake was unaffected by elevated [CO2 ] in both –N and +N
trees.
Leaves were a major sink for new N during the first six
weeks of growth (Figure 6a). In the second half of the growing
season, the leaves lost much of their sink strength, whereas N
partitioning to the stem increased significantly (Figure 6b).
The roots contained a large amount of new N throughout the
experiment and were affected little by the switch in sink
strength from leaves to stem (Figure 6c).
Elevated [CO2 ] had no effect on the partitioning of new N in
+N trees (Figure 6); however, there was a distinct CO2 effect
in –N trees. In the –N;350 treatment, N partitioning to the stem
increased from 11% at Week 6 to 30% at Week 24, whereas N
partitioning to the stem in the –N;700 treatment was much
less, accounting for only 20% at Week 24 (Figure 6b). The decrease in N partitioning to the stem in the –N;700 treatment
was accompanied by increased N partitioning to fine roots,
which accounted for 46% of the total new N in the –N;700
treatment compared with 30% in the –N;350 treatment at
Week 24 (Figure 6c and Table 2).
Discussion
Uptake and partitioning of carbon
Figure 2. Partitioning of new C in (a) leaves and buds, (b) branches
and stem, (c) fine and coarse roots and (d) belowground respiration in
ambient (solid lines, squares) and elevated (dotted lines, circles)
[CO2 ] for +N and –N trees. Means and standard deviation (n = 5).
Nitrogen content and partitioning of new N
Before bud break, N content was 21% less in –N trees than in
+N trees (0.11 versus 0.14 g, Figure 5). The difference in N
In accordance with many studies on the effects of elevated
[CO2 ] on tree growth (see reviews by Curtis and Wang 1998,
Saxe et al. 1998), we observed an increase of about 30% in C
uptake in response to elevated atmospheric [CO2 ] (Figure 1).
In other studies on beech, increases in growth of 53% (Overdieck and Forstreuter 1995) and 27% (Lee and Jarvis 1995)
were found after 1 and 2 years of exposure, respectively, and
Heath and Kerstiens (1997) reported a dry mass increase of
92% after 18 months of exposure to elevated [CO2 ].
Elevated [CO2 ] influenced not only total C uptake, but also
the partitioning of new C. There was a significant shift in C allocation from aboveground to belowground compartments in
response to elevated [CO2 ]. In the +N;350 treatment, 33% of
new C was allocated above ground, but this amount was only
30% in the +N;700 treatment (Table 1). In –N trees, the difference was more pronounced, with 30% of new C allocated
above ground in the –N;350 treatment versus 21% in the
–N;700 treatment. In –N trees, the largest effect of elevated
[CO2 ] was on belowground respiration, where C release was
increased by 70% in the –N;700 treatment compared with the
–N;350 treatment (Table 1). Increased belowground activity
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46
DYCKMANS AND FLESSA
Figure 3. (a) Amount of belowground
respiration and (b) fraction of new C
on total C (RSA) in belowground
respiration under ambient (䊉) and
elevated [CO2 ] (䊐) conditions. Means
and standard deviation (n = 5).
Figure 4. Specific root respiration, calculated as belowground respiration shortly before harvesting divided by the amount of new C in the
fine roots in ambient (䊉) and elevated [CO2 ] (䊐). Means and standard
deviation (n = 5).
in response to elevated [CO2 ] indicates a tendency to increase
soil N uptake to match elevated C supply. This is consistent
with the finding that the shift to belowground C allocation was
especially high in the –N trees. Although this response is
predicted in tree models (Lacointe 2000), many studies have
shown the contrary. For example, Tomlinson and Anderson
(1998) found no effect of elevated [CO2 ] on recent photosynthate partitioning in a 14C tracer study on red oak (Quercus
rubra L.). Vivin et al. (1995) found no effect of elevated [CO2 ]
on root/shoot ratios of pedunculate oak seedlings (Quercus
robur L.) until October, when an aboveground shift was observed. Overdieck and Forstreuter (1995) observed an increase in the root/shoot ratio of beech during the first year of
exposure to elevated [CO2 ], but in subsequent years C was allocated preferentially to the aboveground system. However,
several studies have demonstrated that elevated [CO2 ] increased belowground allocation (Zak et al. 1993 for Populus
Figure 5. Effects of the CO2 and N
treatments on total N content of trees at
Weeks 0, 6, 12 and 24. Means and
standard deviation (n = 5).
TREE PHYSIOLOGY VOLUME 22, 2002
INFLUENCE OF N STORES ON THE REACTION OF BEECH TO ELEVATED [CO2]
47
fine root production of Fraxinus excelsior L. and Quercus petraea L. but had no effect on root/shoot ratios. Based on these
studies, we conclude that the effect of elevated [CO2 ] is dependent on plant nutrient status or external N availability, with
a greater effect toward belowground activity in N-deficient
trees or trees growing in an N-limited substrate.
The large increase in belowground respiration in response
to elevated [CO2 ], especially in the –N treatment (Tables 1
and 2), may be caused by an increase in: (a) fine root mass; (b)
specific root respiration; or (c) fine root turnover, as found by
Pregitzer et al. (1995), resulting in increased microbial respiration. We found no change in specific belowground respiration (calculated as belowground respiration per gram new C in
the fine roots) in response to the treatments (Figure 4) between
Weeks 12 and 24. This suggests that increased belowground
respiration is a result of increased fine root production, as reported by Thomas et al. (2000). Increased belowground respiration relative to new fine root production in the –N treatment
compared with the +N treatment at Week 6 was probably a result of increased formation of fine roots during –N pretreatment. For all treatments, specific root respiration decreased
during the season in response to increasing amounts of fine
roots produced. Increased belowground respiration (together
with increased fine root production) in response to elevated
[CO2 ] was not coupled with a corresponding increase in N uptake.
Uptake and partitioning of nitrogen
Figure 6. Partitioning of new N in +N trees and –N trees growing in
ambient (solid lines, squares) and elevated (dotted lines, circles)
[CO2 ]. (a) Leaves and buds, (b) branches and stem and (c) fine and
coarse roots. Means and standard deviation (n = 5).
grandidentata Michx., Pregitzer et al. 2000 for Populus tremuloides Michx.), but sometimes only when N availability was
low (El Kohen and Mousseau 1994 for Castanea sativa Mill.).
Crookshanks et al. (1998) found that elevated [CO2 ] increased
The RSA of new N was unaffected by elevated [CO2 ] (Tables 1 and 2), but as a result of increased C uptake in response
to elevated [CO2 ] (Figure 1), there was a trend toward decreased N concentrations in the elevated [CO2 ] treatment (Tables 1 and 2). Comparable effects of elevated [CO2 ] and external N supply have been reported for Castanea sativa Mill. (El
Kohen et al. 1992) and two Pinus species (Bassirirad et al.
1997). In both studies, elevated [CO2 ] caused decreasing N
concentrations irrespective of external N supply, whereas elevated [CO2 ] had no effect on tree N content. In a review of the
effects of elevated [CO2 ] on tissue N concentrations, Cotrufo
et al. (1998) concluded that elevated [CO2 ] leads to a decrease
of about 15% in N concentration in trees, even at high N supply. This was interpreted to indicate that elevated [CO2 ] increased nitrogen-use efficiency. Tree N uptake from soil is
mainly driven by N availability rather than by plant internal N
status and N requirement (i.e., previous years N nutrition,
Wendler and Millard 1996, Dyckmans and Flessa 2001). Furthermore, in several studies, a close relationship between N
supply and N uptake (and N tissue concentrations) has been
found (Mackie-Dawson et al. 1994, Proe and Millard 1995,
Kinney and Lindroth 1997, Maillard et al. 2001). These findings suggest that ranking perennial species on the basis of nitrogen-use efficiency may be misleading because, as Johnson
et al. (1995) pointed out, plants that can increase their tissue
nutrient concentrations during periods of high N supply are at
an advantage in habitats where nutrient supply is highly variable or nutrient demand and availability are uncoupled. On the
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48
DYCKMANS AND FLESSA
other hand, Bauer and Bernston (2001) found that N uptake kinetics for Betula alleghaniensis Britt. (but not for Pinus
strobus L.) are more responsive to N supply than to [CO2 ],
provided that N is not over abundant. Moreover, Johnson et al.
(1995) reported that elevated [CO2 ] decreased N concentrations in Pinus ponderosa Laws. irrespective of N fertilization.
We conclude that N uptake by trees is primarily controlled by
soil mineral N availability and that elevated [CO2 ] has only a
small effect on N uptake in most species.
We note that, in contrast to N uptake from the soil, symbiotic N fixation is markedly increased by elevated [CO2 ]; as a
result, N concentrations in N-fixing trees are often found to be
unaffected by CO2 enrichment (Vogel et al. 1997, Olesniewicz
and Thomas 1999, Thomas et al. 2000, Uselman et al. 2000).
Partitioning of new N was unaffected by elevated [CO2 ] in
+N trees. In contrast, in –N trees, partitioning to the stem was
strongly decreased by elevated [CO2 ] and fine roots were a
more important sink in the –N;700 treatment than in the
–N;350 treatment. Increased N allocation to the stem in the
–N;350 treatment relative to the +N;350 treatment is probably
attributable to increased formation of reserves because of a
shortage of C, leading to growth inhibition and a lack of sinks
other than reserves (Dyckmans and Flessa 2001). Our data indicate that elevated [CO2 ] alleviates the C shortage and leads
to increased growth, which in turn reduces the tree’s ability to
form N reserves in the stem. Because growth of beech is
strongly determined by internal N reserves, decreased formation of N reserves in response to elevated [CO2 ] may lead to
down-regulation in the long term. Although Cotrufo et al.
(1998) concluded that N availability had no effect on the response of trees to elevated [CO2 ], low N availability limited
the effect of elevated [CO2 ] in several seedling studies
(Maillard et al. 2001) or under extreme N limitation (Johnson
et al. 1998). This might indicate that internal N reserves are
not only responsible for providing N for tree growth in spring
but may also act as a buffer supplying N to the trees when external N availability is low.
We conclude that the response of beech trees to elevated
[CO2 ] is influenced by tree internal N status. Elevated [CO2 ]
influences C and N partitioning and the tree’s ability to form C
and N reserves for future growth, thus limiting the effect of elevated [CO2 ] on tree growth in the long term. Therefore, in atmospheric CO2-enrichment studies of beech, it is necessary to
take account of the feedback reactions on internal nutrient reserves because the amount of reserves and the ability to form
reserves is an important aspect of the response of beech trees
to a changing environment.
Acknowledgments
The authors thank Bernd Grüning and Lars Szwec for excellent technical support. The research was founded by the DFG (Schwerpunktprogramm “Stoffwechsel und Wachstum der Pflanze unter erhöhter
CO2-Konzentration”). The authors also thank Bernard Ludwig and
Ulrike Sehy for helpful discussions on the paper.
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