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Research

Elevated CO2 increases carbon allocation to the roots of

Blackwell Science Ltd

Lolium perenne under free-air CO2 enrichment but not in

a controlled environment
Daniel Suter1, Marco Frehner1,2, Bernt U. Fischer1, Josef Nösberger1 and Andreas Lüscher1,3
1
Institute of Plant Sciences, Swiss Federal Institute of Technology (ETH), Universitätstrasse 2, CH–8092 Zurich, Switzerland; 2Present address: CRINA SA,
Chemin de la Combe 15, CH–1196 Gland, Switzerland; 3Present address: Swiss Federal Research Station for Agroecology and Agriculture (FAL),
Reckenholzstrasse 191, CH–8046 Zurich, Switzerland

Summary

Author for correspondence: • Grass swards often show a higher root–shoot ratio of dry matter (R : SDM) at
Andreas Lüscher elevated [CO2] than at ambient [CO2]. However, it is not known whether this is a
Tel: +41 (0)1377 72 73
result of a sustained increase in C allocation to the roots.
Fax: +41 (0)1377 72 01
Email: [email protected] • The effects of free-air CO2 enrichment (FACE) on carbon allocation to roots
in established Lolium perenne (perennial ryegrass) swards during regrowth were
Received: 2 August 2001
investigated by means of 14C labelling and compared with data from a controlled
Accepted: 29 November 2001
environment experiment.
• Elevated [CO2] in the field increased root dry matter (109%), R : SDM (44%)
and, in accordance, root–shoot 14C ratios (R : S14C, 39%), as well as the intercept of
the allometric line. By contrast, elevated [CO2] did not affect the allometry of the
plants under controlled conditions. However, at low N concentration in the nutrient
solution, the R : SDM and the intercept of the allometric line increased.
• It is suggested that the remarkably different responses to elevated [CO2] under
field and controlled conditions result from differences in both N availability for
growth, and C sink strength of the shoots.

Key words: Lolium perenne (ryegrass), elevated CO2, free-air CO2 enrichment
(FACE), biomass partitioning, root–shoot ratio, allometry, carbon allocation, 14C
pulse labelling.

© New Phytologist (2002) 154: 65–75

Schapendonk et al., 1997; van Ginkel et al., 1997), due mainly

Introduction to an increase in root DM. Assessments of the R : SDM
Since the beginning of industrialization, the atmospheric allometry of seedlings grown in short-term experiments in
partial pressure of CO2 (p CO2) has been steadily increasing controlled environments revealed that ontogenetic drift
from 27 Pa to its present value of 36 Pa CO2. Models predict may be responsible for a shift in R : SDM at elevated p CO2
that the atmospheric p CO2 will increase to about 70 Pa CO2 (Baxter et al., 1997; Lutze & Gifford, 1998; Stirling et al.,
in the second half of the twenty-first century (Houghton 1998). However, it was not clear whether older cut plants
et al., 1996). Grasslands account for a considerable land area still show a higher R : SDM at elevated p CO2 during regrowth.
(FAO, 1995) and are considered to have a high CO2 sink At elevated p CO2 under field conditions, Lolium perenne
capacity (Parton et al., 1995). Thus, grasslands are suggested exhibited a strong increase in single-leaf photosynthesis
as playing an increasingly important role in the earth’s carbon (Rogers et al., 1998; Isopp et al., 2000) but only a weak
cycle. increase in yield (Hebeisen et al., 1997; Suter et al., 2001).
Various experiments have shown that grass plants exhibit This discrepancy may be explained in part by a greater pro-
a higher root–shoot ratio (R : SDM) when grown at elevated portion of fixed C that is allocated to unharvested plant parts.
p CO2 (Farrar & Williams, 1991; Rogers et al., 1996; Soussana Well-established swards under field or field-like conditions
et al., 1996; Cotrufo & Gorissen, 1997; Hebeisen et al., 1997; also show a higher R : SDM at elevated p CO2 (Hebeisen et al.,

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66 Research

1997; Schapendonk et al., 1997; Suter et al., 2001). It was not from 18 to 47 mg K kg–1 soil, respectively (Lüscher et al., 1998).
clear, however, whether this increase in root DM of field- To maintain nonlimiting levels of phosphorus and potassium
grown swards was solely a result of: (1) a larger amount of in intensive grassland, 4.3 g P m–2 yr–1 and 24.6 g K m–2 yr–1
undecomposed ( Jongen et al., 1995) dead roots together with were applied once per year in spring. The annual amount of
an unchanged amount of live roots at elevated p CO2; or (2) N fertilizer was 56 g N m–2, which is markedly higher than
an increase in root longevity (Eissenstat et al., 2000; Pritchard the 15–30 g N m–2, typical of grasslands in this region. The
& Rogers, 2000), resulting in a slower turnover rate of the portions of N applied during the growing season were adjusted
root DM pool. In both cases, despite a greater root DM, the to the expected DM production in each regrowth period, as
C supply to the root fraction could be unaffected by elevated described by Zanetti et al. (1996): highest in spring and
p CO2. Thus, the question arose: How does the allocation of lowest towards the end of the growing season. Nitrogen
C in (1) field-grown swards and (2) plants in a controlled was applied as NH4NO3 every 4 wks beginning at the start of
environment change at elevated p CO2? In order to answer the growing season. Table 1 lists the meteorological data.
this question, the C allocation in the plant must be deter- During the observation period the temperature was about
mined. Single measurements at the end of a regrowth period 0.5°C above and the precipitation about 45% below the
or average values of the regrowths in a growing season may 1993–99 average. The sum of global radiation was at about
mask dynamic processes in C allocation during a particular average.
regrowth period.
In order to elucidate the effect of elevated p CO2 on C Preparation and treatments A sward of Lolium perenne, which
allocation in grassland ecosystems, the dynamics of 14C parti- grew under FACE conditions for more than 3 yr, was removed
tioning was examined in Lolium perenne (perennial ryegrass) by applying glyphosate [N-(phosphonomethyl)glycine] followed
model swards in the Swiss FACE (free-air carbon dioxide by shallow tillage in mid-July in 1996. Individual plants
enrichment) facility during a vegetative regrowth period. In a of Lolium perenne L. cv. Bastion, a widely used forage plant
second experiment, the dynamics of root and shoot growth of species in temperate regions, were sown in 15-ml pots in soil
regrowing spaced plants on a sand culture with nutrient taken from the FACE area at the beginning of the last week
solution were examined in controlled environment chambers in July and grown in a greenhouse for 6 wks. In the first week
to elaborate the effect of contrasting experimental conditions. of September, the plants were transplanted to the main plots
(9.24 × 3.15 m) at a spacing of 7 cm (204 plants per m2).
The swards were cut 5 cm above the ground in the first
Materials and Methods week of November. In the spring of 1997 and 1998, all the
plots were weeded by hand before the onset of the growing
Field experiment
season.
Experimental site The field experiment was conducted in The experiment was designed as a split-split-plot with three
the Swiss FACE array (Hebeisen et al., 1997) at Eschikon blocks. The blocks were set up according to the crops grown
(8°41′ E, 47°27′ N) near Zurich, 550 m above sea level. The in the year preceding the installation of the FACE facility
soil, an eutric cambisol, consisted of about 36% sand, 33% (4 yr before the start of the experiment described here). These
silt and 28% clay and was a clay loam. The organic matter crops were winter wheat (blocks one and three) and grass/
content varied from 2.9 to 5.1% and the pH (water extracted) white clover mixture (block two). The main plot treatment
ranged from 6.5 to 7.6. The available P and K (CO2-saturated was p CO2. The levels of p CO2 were ambient (36 Pa) and
water extractable) ranged from 1.2 to 6.0 mg P kg–1 soil and elevated (60 Pa). The latter was obtained by using the FACE

Table 1 Weekly average of daily mean

Temperature Precipitation Global radiation temperature, sum of precipitation and sum of
Date (°C) (mm) (MJ m–2) global radiation in the FACE experiment at
Eschikon, Switzerland, immediately before
30 June– 6 July 16.6 14.0 120.7 and during the regrowth period examined in
7–13 July 17.2 2.3 111.1 summer 1998
14 –20 July 19.3 8.1 154.4
21– 27 July 21.2 32.1 130.6
28 July– 3 August 17.7 20.6 95.2
4–10 August 20.9 0.0 157.1
11–17 August 22.3 0.1 155.9
18 – 24 August 17.3 47.8 91.4
25 – 31 August 13.0 0.0 131.8
Mean 18.4 – –
Sum – 125.0 1148.2

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Research 67

technique, as described by Lewin et al. (1992). Briefly, three carried labelled CO2 into the cuvette, which was vented to the
fumigated circular areas (18 m diameter) were installed in the environment. A small battery-powered fan inside the cuvette
spring of 1993. Three nonfumigated control areas of the same prevented condensation on the surface of the cuvette and
size were established at the same time. Fumigation was done mixed the labelled CO2 with the air. The injections were
by a circular array of 32 vertical vent pipes, which were fed repeated at 1-min intervals. The cuvette was removed 1 min
with CO2-enriched air through a 18-m toroidal distribution after the last injection (t30). The labelling procedure usually
tube. The valves of the vent pipes were computer controlled. started at 10 : 00 hours and was conducted simultaneously in
At wind speeds of more than 0.4 m s–1 only the valves of the both CO2 treatments of the same block. The order of labelling
pipes on the windward side were opened. The CO2-enriched of the differently treated plots was randomized per block but
air was, thus, distributed over the experimental area by the wind. was the same in both pCO2 treatments of the respective
At wind speeds below 0.4 m s–1 the valve of every second vent block. One block was labelled each day. Labelling took place
pipe was opened. An infrared gas analyser, connected to a on 20–22 July, 3–5 August, 17–19 August and 31 August to
computer, continuously measured the actual pCO2 in the 2 September in 1998.
air, which was sampled in the centre of the experimental area,
0.1 m above the canopy. Over the whole experimental period, Data collection and measurements Measurements were made
the 1-min averages of p CO2 were within the target p CO2 of after 14, 28, 42 and 56 d of regrowth from 22 July to 4 Sep-
60 ± 6 Pa for 90–94% of the fumigation time, depending on tember 1998. The plant material from an area of 0.21 × 0.21 m
the ring. The seasonal average of the p CO2 was 60 ± 0.2 Pa. (sub-subplot) was harvested destructively 46 h after pulse
Fumigation was continuous during daylight hours and lasted labelling. The shoot material was divided into stubble
from spring until November when the air temperature was at (below cutting height) and yield (above cutting height), using
least 5°C (2 m above the ground), assuming that plant growth a stratified clipping technique. The above-ground plant
was marginal and that CO2-induced effects on photosynthesis material was harvested using a metal frame to ensure exact
were weak at low temperature (Long, 1994). There was a dis- cutting height. The roots were sampled to a depth of 10 cm
tance of at least 100 m between fumigated and control areas (0.21 × 0.21 m), which accounts for 85–90% of the total
in order to eliminate the possibility of interactions among the root mass of Lolium perenne below the sampling area at
areas, (e.g. ambient areas being affected by elevated pCO2). the experimental site (Hebeisen, 1997), and the roots were
Each area contained one main plot. washed carefully. Furthermore, elevated pCO2 did not affect
Pretreatments were applied during the establishment of the the vertical distribution of the roots (Zimmermann, personal
swards and until the observations started in the summer of communication). Harvested sub-subplots were replaced by turfs
1998 in order to produce plants of different morphology. The from the same pretreatment to avoid gaps in the subplots.
pretreatments were combinations of cutting height (4 cm and Green and necrotic (visually determined) plant material from
8 cm) and cutting frequency (intervals of 4 wks and 8 wks, each fraction were separated. The plant material was heated in
resulting in eight and four cuts per year, respectively) and were a microwave oven (Popp et al., 1996) to stop any enzymatic
randomly assigned to the four subplots (2.31 × 3.15 m) activity and dried in a ventilated oven at 65°C for 48 h.
within each main plot. Four sub-subplots (0.21 × 0.21 m,
14C
surrounded by a 0.21-m border) were randomly chosen from analysis The plant material was ground in a sample mill
each subplot. The sub-subplots were used for destructive (Tecator Cyclotec 1093, Tecator AB, Höganäs, Sweden) and
harvests and for 14C pulse-labelling. processed further in a ball mill (Retsch MM2, Schieritz und
Hauenstein AG, Arlesheim, Switzerland). The powdered
14C pulse-labelling In the established sward in the field, sample (22.5 ± 2.5 mg) was put into a 20-ml glass vial
changes in the size of the big pool of roots, consisting of (Packard Instrument Company, Meriden, CT 06450, USA)
growing and old dying roots, do not represent C allocation to and a suspension of 4 mg cellulase (crude powder from
the roots. In order to measure C allocation to the roots, 14C Trichoderma viride) and 4 mg maceroenzyme (pectinase,
pulse-labelling was carried out. Just before the start of the crude powder from Rhizopus sp.) in 200 µl phosphate buffer
labelling of the sub-subplot, 1 ml of 9.25 MBq 14C Na2CO3 (2 mM NaH2PO4, 0.5 mM CaCl2, pH 6) was added. The
solution (50 mM Tris, pH 7) and 29 ml distilled H2O were capped vials were placed on a shaker and incubated at 37°C
drawn into a syringe. At the start (t0) of labelling, 1 ml of for 20 h. One millilitre of Soluene-350 (Packard Instrument
the diluted solution was injected into a 50-ml reaction tube Company) digesting solution was added to each vial, and
containing 5 ml of lactate (85% in H2O). A pump connected the re-capped vials were incubated again at 37°C for 20 h.
to the reaction tube blew air (10 l min–1) from the sur- After incubation and after the samples had reached
roundings (intake at a distance of about 0.5 m from the ambient temperature, 15 ml Hionic-Fluor (Packard Instrument
sub-subplot) through the solution in the reaction tube and Company) were added to each sample. The vials were capped
into the Plexiglas labelling cuvette (0.35 × 0.35 × 0.4 m), and shaken to homogenise the digested and dissolved plant
which was placed over the sub-subplot; the stream of air material before liquid scintillation counting (Packard 2500TR,

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68 Research

Packard Instrument Company). Vials without plant material irrigated twice a day with a nutrient solution containing
and enzymes were used to determine the 14C background. 7.5 mM NO3– (Hammer et al., 1978). Iron (0.124 mM
Internal standards with a known amount of 14C were used to EDTA ammonium iron(III)salt; Fluka, Buchs, Switzerland)
correct for quenching. was supplied without adjusting the pH. Plants and pCO2
treatments were rotated between growth chambers each
Allometry Logarithmic shoot DM (sum of stubble and yield) week.
was plotted against logarithmic root DM. The allometric After 17 d, vigorous plants with one tiller and two to
relation was obtained as the linear regression function in the three leaves were selected in each pCO2 treatment, trimmed
double log plot (Farrar & Williams, 1991; Baxter et al., to 5.5 cm of shoot and 2.5–3 cm of roots and transplanted
1994). This line shows the relative growth rates of C- singly into cylindrical pots 7 cm in diameter and 25 cm
acquiring tissue (shoot) in relation to the relative growth rates high, filled with 1.5 kg of silica sand, as described earlier. The
of nutrient-acquiring tissue (root) of the sward and is level of elevated pCO2 was increased to 70 Pa. Over the whole
expressed as experimental period, the average of the low pCO2 was
35 ± 0.8 Pa for 96% of the time and the average of the high
Loge(root DM) = b + k Loge(shoot DM). pCO2 was 60 ± 0.9 Pa and 70 ± 1.1 Pa (before and after
planting in individual pots, respectively) for 95% of the
Statistical analysis The statistical analysis was carried out fumigation time. In order to guarantee a controlled nutrient
using the GLM procedure of the SAS package (SAS Institute, supply, pure silica sand and nutrient solution were chosen to
1996). The model was a split-split-plot with pCO 2 as avoid N sequestration/mineralization, which may occur in
the main plot factor; thus, pCO2 was tested with the field soil. Nutrient solution (30 ml) was added to each pot
pCO2 × block interaction as the error term. This is a weak twice per day. The N concentration was changed to the experi-
test, and pCO2 effects are more readily detected by the mental levels 39 d after sowing. Within each of the six
dynamics of the response of the pretreatment effects to replicates, plants were randomly allocated to sampling dates.
elevated p CO2 (e.g. pCO2 × cutting frequency × sampling Nutrient solutions were prepared according to (Hammer
date and pCO2 × cutting height × sampling date). Dry et al., 1978), without adjusting the pH, using 0.124 mM
matter data and root–shoot ratios were Loge transformed EDTA ammonium iron(III)salt (Fluka) as a source of iron.
before the analysis of variance in order to obtain normal The solution was modified as follows: in the low-N regime,
distribution and homogeneity of variance. The reported the KNO3 and Ca(NO3)2 were replaced by 0.5 mM KCl,
means were obtained by back-transformation. For all the 1 mM K2SO4, 0.5 mM Ca(NO3)2 and 2 mM CaSO4 (final
traits examined, the cutting height affected neither the concentration of NO3− was 1 mM); in the high-N regime
response to CO2, nor the response to cutting frequency. Thus, the concentration of Ca(NO3)2 was changed to 6.25 mM
the data of cutting height were pooled. The linear regression (final concentration of NO3− was 15 mM, a concentration
functions for the different pCO2 treatments were compared that provides ample N under these experimental conditions).
using Fisher’s t-test (Zar, 1984). Pots were flushed with adequate amounts of deionized water
before the first application of new nutrient solutions (100 ml
per pot twice a day). To ensure a nonlimiting water supply
Controlled environment experiment
with increasing plant size, the amount of nutrient solution
Plant material and growth conditions Lolium perenne L. cv. was increased to 150 ml per pot (twice a day) 63 d after
Bastion plants were grown from seed in boxes filled with silica sowing.
sand (particle size 0.7–1.2 mm) to 5 cm and placed in
Conviron PGV 36 controlled environment chambers Sequential harvests during regrowth Forty-five days after
(Conviron, Winnipeg, Manitoba, Canada) set at 35 or 60 Pa sowing (28 d after transplanting into pots), plants were defoliated
pCO2. The levels of p CO2 were monitored by WMA-2 to 4 cm above the ground. Regrowth was monitored at four
infrared gas analysers (PP-Systems, Hitchin, Herts, UK). harvests, 7, 11, 17 and 28 d after defoliation. For each harvest,
Excess CO2 was removed by forcing air through soda lime one set of plants, consisting of six replicates, was sampled.
pellets (Roth, Karlsruhe, Germany). The daylength was set The sand was carefully removed and the plants separated
to 16 h with 12 h at maximum PPFR (500 µmol m–2 s–1 at into roots, stubble (leaf sheaths and enclosed parts of the
the pot level). The PPFR was increased and decreased at growing leaf ), yield and necrotic tissue. Leaves were classified
2-h intervals at the beginning and end of the day, respect- as necrotic when more than two-thirds of their area had
ively. Very high-output cool white fluorescent tubes senesced. The dry weight of oven-dried (48 h at 65°C)
(Osram Sylvania Inc., St Marys, PA, USA) and incandescent material was determined. Since the root pool contained
bulbs (Osram Sylvania Inc.) were used to obtain the desired young roots only, the relative increase in root weight to shoot
PPFR. Relative humidity was maintained at 80%. Air tem- weight in these young plants is taken as a measure of C
perature was set to 18°C/13°C (day/night). Plants were allocation (no 14C labelling).

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Research 69

Statistical analysis Dry matter and root–shoot ratios were

Loge transformed before statistical analysis in order to obtain
Results
normal distribution and homogeneity of variance. Means shown
Dry matter
were obtained by back-transformation. Statistical analyses were
carried out using the GLM procedure of the SAS statistical In the field experiment, averaged over the whole observation
analysis package (SAS Institute, 1996). The experiment was a period, total DM at elevated pCO2 (977 g m–2) was 65%
complete randomized block design; the factors CO2, N and higher (P < 0.05) than DM at ambient pCO2 (Fig. 1a). This
sampling date were varied, and each treatment was replicated six CO2-induced difference was mainly due to a 109% increase
times. The linear regression functions for the different pCO2 (P < 0.05) in root DM, from 184 g m–2 at ambient pCO2 to
and N levels were compared using a Fisher’s t-test (Zar, 1984). 384 g m–2 at elevated pCO2 (Fig. 1b), and to a 53% increase

Fig. 1 (a–d) Development of total DM

(a), DM of roots (b), stubble (c) and yield (d)
during 56 d of regrowth of 2-yr-old field-
grown Lolium perenne swards at ambient
(36 Pa, open symbols) and elevated (60 Pa,
solid symbols) pCO2 and after infrequent
(four cuts per year, circles) and frequent
(eight cuts per year, triangles) cutting
treatments before the examined regrowth.
(e–h) Total DM (e), DM of roots (f), stubble
(g) and yield (h) during 28 d of regrowth of
spaced Lolium perenne plants grown in a
controlled environment on sand culture with
nutrient solution containing low N (1 mM
NO3–, hexagons) or high N (15 mM NO3–,
squares) at ambient (35 Pa, open symbols)
and elevated (70 Pa, solid symbols) pCO2.
Error bars = SE, n = 6.

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70 Research

(P < 0.05) in stubble DM, from 310 g m–2 at ambient pCO2 1.0
to 473 g m–2 at elevated pCO2 (Fig. 1c). The yield DM (a)

Root DM : shoot DM
(Fig. 1d) exhibited a 378% increase (P < 0.0001) during
0.8
regrowth; it showed 30% higher values at elevated pCO2, but
this difference was not significant.
0.6
In the controlled environment experiment, total plant
DM (Fig. 1e) increased (P < 0.0001) by 1100% during
regrowth. Averaged over the whole observation period,
0.4
54% more DM (P < 0.0001) was measured at elevated
pCO2 than at ambient pCO2. The responses of the DM 0.2
(Fig. 1f–h) of the yield (60%), stubble (43%) and roots
(47%) to elevated pCO2 over the observation period were 0.0
all highly significant (pCO2 P < 0.0001). Plants grown 14 28 42 56 Mean
under a high-N regime exhibited 130% more (P < 0.0001)
total plant DM than low-N plants (Fig. 1e). A greater N Day
availability also significantly increased the DM (Fig. 1f–h)
of yield (195%), stubble (205%) and roots (27%). The 1.0
(b)
Root DM : shoot DM
response of total DM to elevated pCO2 was not affected by
the N treatment. 0.8

0.6
Root–shoot ratio
During regrowth of the field-grown swards the root–shoot 0.4
ratio of the DM (R : SDM) (Fig. 2a) decreased significantly
(P < 0.0001), from 0.94 on day 0 (data not shown) to 0.70 0.2
after 14 d of regrowth and to 0.46 by the last sampling
after 56 d. The R : SDM was 44% higher at elevated pCO2 0.0
than at ambient p CO2 and the response to pCO2 depended 7 11 17 28 Mean
on the cutting frequency before the experimental period
(p CO2 × frequency, P < 0.05). Infrequently pretreated swards Day
exhibited a 29% (P < 0.01) increase in R : SDM, frequently Fig. 2 Root–shoot ratio of DM (R : SDM) (a) during 56 days of
pretreated swards showed a pCO2-induced increase in the regrowth of 2-yr-old field-grown Lolium perenne swards at ambient
R : SDM of 60% (pCO2, P < 0.0001). The response of R : SDM (36 Pa, open symbols) and elevated (60 Pa, solid symbols) pCO2 and
after infrequent (four cuts per year, circles) and frequent (eight cuts
to elevated p CO2 did not change throughout the regrowth
per year, triangles) cutting treatments before the examined regrowth
period. and (b) during 28 d of regrowth of spaced Lolium perenne plants
The R : SDM of regrowing Lolium perenne plants in the grown in a controlled environment on sand culture with nutrient
growth chamber (Fig. 2b) depended on the sampling date solution containing low N (1 mM NO3–, hexagons) or high
(P < 0.0001). The plants showed the highest R : SDM value N (15 mM NO3–, squares) at ambient (35 Pa, open symbols) and
elevated (70 Pa, solid symbols) pCO2. Error bars = SE, n = 6.
(0.48) on the first sampling date of the experiment. Sub-
sequently, they exhibited significantly lower R : SDM values
(0.37–0.43). Averaged over the entire regrowth period, elevated The response of R : S14C to elevated pCO2 did not change
p CO2 did not affect the R : SDM (pCO2, ns). Plants grown in throughout the experimental period.
a high-N regime exhibited a 52% lower (P < 0.0001) R : SDM The root–shoot ratio of 14C distribution depended on the
than plants grown in a low-N regime. Elevated pCO2 did not root–shoot DM ratio, both of which decreased with the
affect this relationship (p CO2 × N, ns). increasing length of regrowth (Fig. 4). This relationship did
not depend on pCO2, as demonstrated by the comparable
slope and intercept of the regression curves of the two pCO2
Root–shoot ratio of 14C distribution
treatments (t-test for pCO2, ns).
The sampling date had a significant (P < 0.01) effect on the
root–shoot ratio of the 14C distribution (R : S14C) of the field-
Root–shoot allometry
grown Lolium perenne swards (Fig. 3); it decreased from 0.12
on the first sampling date after 14 d to 0.08 after 56 d of Under field conditions, elevated pCO2 led to a significant
regrowth. The R : S14C averaged over all the sampling dates displacement of the allometric regression line (Fig. 5a). This was
was significantly higher (39%) at elevated pCO2 (P < 0.01). resulted from an increase (P < 0.001) in the intercept b, revealing

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Research 71

0.20 favour of the shoot compared with the low-N regime. This
difference was manifested by a significantly smaller intercept
Root 14C : shoot 14C

b of the allometric regression lines (t-test for b, P < 0.01) in the

0.15 high-N regime.

0.10 Discussion

0.05 Sustained increase in C allocation to the roots in the field

The two most important results of these experiments are:
0.00 (1) in well-established 2-yr-old Lolium perenne swards under field
conditions there was a sustained increase in C allocation to the
14 28 42 56 Mean roots in response to elevated pCO2; and (2) under controlled
Day conditions no change in C allocation occurred. A higher
14C
R : SDM of field-grown grass swards at elevated pCO2 is in line
Fig. 3 Root–shoot ratio of 46 h after pulse labelling (R : S14C)
during 56 d of regrowth of 2-yr-old field-grown Lolium perenne with other experiments (Soussana et al., 1996; Hebeisen et al.,
swards at ambient (36 Pa, open symbols) and elevated (60 Pa, solid 1997; Schapendonk et al., 1997). It was not known, how-
symbols) pCO2 and after infrequent (four cuts per year, circles) and ever, whether this is due to (1) an ontogenetic drift, (2) less
frequent (eight cuts per year, triangles) cutting treatments before the decomposition of the roots, (3) an extended longevity of roots
examined regrowth (error bars = SE, n = 6).
or (4) a sustained increase in C allocation to the roots. The fact
that 14C allocation to the roots remained higher at elevated
0.20 pCO2 (Fig. 3), even 2 yr after planting, demonstrates that this
increase in C allocation to the roots under field conditions was
a sustained effect to atmospheric CO2 enrichment.
The intercepts b of the allometric lines (Fig. 5a) of the field
C

0.15
14

experiment data reveal that at elevated pCO2 more root DM

C : shoot

per unit shoot DM is produced. This pCO2-related effect did

not depend on the change in shoot size, because the slope k of
0.10 the allometric line was not significantly affected by elevated
pCO2. The remarkable absence of an ontogenetic drift in
14

R : SDM confirmed the findings of the 14C labelling. The

Root

greater intercept b in the field at elevated pCO2 compared

0.05 with ambient pCO2 and the constant slope of the allometric
line convincingly show that a significant adjustment to elevated
pCO2 may occur in swards under field conditions.
0.00 The uniformity of the relationship between R : SDM and
0.00 0.25 0.50 0.75 1.00 R : S14C at both pCO2 levels suggests that carbon costs per
unit root DM were not affected by elevated pCO2. Combined
Root DM : shoot DM with the marked increase (by 109%) in root DM at elevated
Fig. 4 Root–shoot ratio of DM (R : SDM) of Lolium perenne pCO2, our field experiment revealed a strong increase in C
plotted against the root–shoot ratio of 14C 46 h after pulse labelling costs of the total root system. These increased costs help to
(R : S14C). Data collected throughout 56 d of regrowth of 2- yr-old
field-grown Lolium perenne swards at ambient (36 Pa, open
explain the discrepancy between a 50% increase in the photo-
symbols) and elevated (60 Pa, solid symbols) pCO2 (n = 6) synthesis of single Lolium perenne leaves (Rogers et al., 1998;
(R : S14C = – 0.00338 + 0.17 × R : SDM, r 2 = 0.82, P < 0.0001). (The Isopp et al., 2000) and the small, often statistically nonsigni-
R : SDM and R : S14C are derived from Figs 2a and 3, respectively.) ficant, yield response of Lolium perenne swards in the same
FACE array (Hebeisen et al., 1997; Suter et al., 2001; see also
a greater amount (plus 52%) of root DM per unit shoot DM Fig. 1d).
produced at elevated pCO2 than at ambient pCO2. The slope Higher C costs of the root fraction are in line with findings
k of the allometric curves did not significantly change. of other experiments, in which higher carbon costs were indi-
Under controlled conditions (Fig. 5b), there was no differ- cated by an increase in below-ground respiration related to
ence between the root–shoot allometric relationships of the an increased root DM at elevated pCO2 (Billes et al., 1993;
two pCO2 levels (t-test for both slope k and intercept b: ns), van Ginkel et al., 1997; Schapendonk et al., 1997).
as clearly indicated by the congruent regression lines. The The data on 14C allocation in favour of the root do not
high-N regime led to a change in the root–shoot allometry in enable us to determine whether or not the C is used for (1) new

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72 Research

7
(a)
Loge root (g m–2 )

4
5.4 5.6 5.8 6.0 6.2 6.4 6.6
Log e shoot (g m–2 )

2 Fig. 5 Allometry of root and shoot DM obtained (a) during

(b)
Loge root (g plant –1)

56 d of regrowth of 2-yr-old field-grown Lolium perenne

1 swards at ambient (36 Pa, open symbols) (Loge(root
DM) = 1.95 + 0.08 × Loge(shoot DM), r 2 = 0.01, P < 0.785)
and elevated pCO2 (60 Pa, solid symbols) (Loge(root
0 DM) = 1.56 + 0.40 × Loge(shoot DM), r 2 = 0.11, P < 0.296)
and following infrequent (four cuts per year, circles) and
–1 frequent (eight cuts per year, triangles) cutting treatments
before the examined regrowth (n = 6) and (b) during 28 d
of regrowth of spaced Lolium perenne plants grown in a
–2 controlled environment on sand culture with nutrient solution
containing low N (1 mM NO3–, hexagons) (Loge(root DM) =
–3 –0.56 + 1.05 × Loge(shoot DM), r 2 = 0.90, P < 0.0001)
or high N (15 mM NO3–, squares) (Loge(root DM) =
–2 –1 0 1 2 3 4 –1.16 + 0.90 × Loge(shoot DM), r 2 = 0.96, P < 0.0001) at
ambient (35 Pa, open symbols) and elevated (70 Pa, solid
Log e shoot (g plant –1) symbols) pCO2.

growth of roots in relation to an increased root turnover the R : SDM and the allometry. This demonstrates that the
(Fitter et al., 1996; Loiseau & Soussana, 1999), (2) higher response of DM allocation to elevated pCO2 of plants in a
specific root activity (BassiriRad, 2000) or (3) larger amounts sward under field conditions and of individual plants in
of root exudates (Grayston et al., 1998). All these processes growth chambers is clearly different.
may change the quantity (Ineson et al., 1996; Leavitt et al., Which factors are responsible for the observed differences?
1996) and quality ( Jongen et al., 1995; Hartwig et al., 2000; In the same FACE array the response of Lolium perenne to
Daepp et al., 2001) of the C input into the soil under elevated elevated pCO2 has been shown to be N-limited except when
pCO2. This may be the cause of changes in the number and extremely large amounts (112 g m–2 yr–1) of N fertilizer were
the population structure of soil and rhizosphere microorgan- applied (Daepp et al., 2001). Under a nonlimiting supply of
isms (Cotrufo & Gorissen, 1997; Paterson et al., 1997; N in the field, the harvest index and the R : SDM of Lolium
Sadowsky & Schortemeyer, 1997; Marilley et al., 1999). Such perenne were not affected by elevated pCO2 (Daepp et al., 2001).
a change could influence the C flux through the plant–soil Thus, the swards in our field experiment, which were supplied
system, because microorganisms are involved in the decom- with 56 g N m–2 yr–1, were considered to be N-limited.
position of plant-derived C-containing compounds as well as Elevated pCO2 leads to faster growth of the plant, which
in the sequestration of C (Berntson & Bazzaz, 1996; Paterson increases the need for N. Thus, the increased partitioning of
et al., 1997) and nutrient cycling. C to the roots may be a reaction of the plant to meet the
greater N demand by investing in N-acquiring tissue until the
C supply is balanced by acquired N (Brouwer, 1983; Chapin
Effect of elevated pCO2 on C alloction depended
et al., 1987; Schenk et al., 1996; Soussana et al., 1996).
strongly on the experimental conditions
Numerous experiments on N supply and plant growth
In contrast to the field experiment, elevated pCO2 in the have been conducted with grass species. Nitrogen shortage
experiment under controlled conditions had no effect on led to an increase in C allocation to the root fraction (Lutze

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Research 73

& Gifford, 1998; Arredondo & Johnson, 1999; Glimskär ontogenetic effect (Hunt et al., 1995; Lutze & Gifford, 1998;
& Ericsson, 1999; Mackie-Dawson, 1999; Paterson & Sim, Harmens et al., 2000) related to an increase in the R : SDM
1999), as observed in our controlled environment experi- with increasing developmental stage (size) combined with a
ment, independent of atmospheric pCO2. By contrast, in the faster growth of the plant under elevated pCO2 (Gedroc et al.,
high-N treatment in the controlled environment experiment 1996; McConnaughay & Coleman, 1999). Thus, if plotted
the plants were not limited by N in either of the CO2 treat- allometrically, this CO2 effect disappears. These plants were
ments. Thus, elevated pCO2 had no effect on the R : SDM. In very young seedlings which exhibit a strong change in R : SDM
the low-N treatment in the controlled environment experi- with increasing developmental stage. In our controlled envir-
ment, the growth of the plants was N-limited, even at ambi- onment experiment, however, the plants were already well-
ent p CO2. This is clear from the much lower DM production established when the measurements were taken (first harvest
compared with the high-N treatment. However, the increase 52 d after sowing). Thus, there was no important change in
in the R : SDM caused by low N showed that the roots reacted the R : SDM during the experimental period, independent of
to environmental changes in the controlled environment. pCO2. As a result, the higher absolute growth rate at elevated
Furthermore, the plants increased their root mass at both pCO2 (Fig. 1e) did not have an effect on R : SDM. There is
levels of CO2 and N throughout the experimental period. Thus, some evidence that the effect of elevated pCO2 on k is species
it is unlikely that the pot size was responsible for the lack of dependent. For example, Crookshanks et al. (1998) reported a
an R : SDM response to elevated p CO2 (McConnaughay et al., significant enhancement of the k-value of the R : S allometry
1993). in Arabidopsis thaliana seedlings. Baxter et al. (1994) found a
The difference between the unchanged R : SDM in the sand CO2-induced change in the allometric coefficient in favour of
culture in the low-N treatment and the pCO2-induced the shoot in Festuca vivipara, while they did not find a change
changes in the field, both at limiting N supply, may be caused in the R : S allometry of Poa alpina and Agrostis capillaris.
by the different supply of nutrients. In the sand culture, the In conclusion, well-established L. perenne swards showed
nutrient supply was steady, because of the regular application a sustained increase in the C allocation to the roots related to
of nutrient solution. The plants therefore met their additional a change in the DM allocation in favour of the roots under
N demand, which was caused by an increase in the supply of elevated pCO2 in the field. In contrast, plants grown in a con-
C. By contrast, the field experiment was fertilized only once trolled environment showed no such change in the R : SDM.
in 28 d. This may have led to less N being available for several The causes of the different responses to elevated pCO2 may
days. Furthermore, a greater amount of nutrients may have be N availability, the age of the plants and C-sink strength of
been immobilized by soil microorganisms because of a higher the shoot. The sustained greater C allocation to the roots at
C : N ratio in the ecosystem at elevated pCO2 (Díaz et al., elevated pCO2 may have pronounced effects on the yield of
1993). Lolium perenne as well as on many processes in the soil.
Another reason for the higher R : SDM at elevated pCO2
under field conditions, but not under controlled conditions,
may be a C-sink limitation of the shoot in the dense sward Acknowledgements
because of, for example, the poor growth of new tillers (Suter We thank W. Wild, W. Wasiak and U. Rossel for technical
et al., 2001). The roots tend to compete less efficiently for assistance and H. Blum, R. Bossi, J. Nagy, and G. Hendrey for
C than the shoot (Donaghy & Fulkerson, 1998; Mackie- maintaining the FACE. We specially thank K. Girgenrath and
Dawson, 1999) and, as a consequence, carbohydrate avail- the laboratory of organic chemistry at the ETH for con-
ability for root growth may be better when the shoot sink is ducting the 14C analyses. M. Schoenberg checked the English.
weak. This may also explain why the response of R : SDM to The Swiss FACE was supported by the Swiss Federal Institute
elevated p CO2 was stronger in the frequently pretreated of Technology, the Swiss National Energy Research Fund, the
swards than in the infrequently pretreated swards. The shoots Swiss National Science Foundation, the Swiss Department
of single young plants in the controlled environment experi- for Energy, the Swiss Department for Agriculture and the
ment were not spatially restricted, as demonstrated by the Brookhaven National Laboratory (NY, USA).
site filling of these Lolium perenne plants, which was at a
maximum at both pCO2 levels (Fischer, 1998). Farrar & Jones
(2000) hypothesize that C allocation may be controlled by References
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