ORIGINAL ARTICLE OA
Functional
Ecology 1999
13 (Suppl. 1),
3–11
000
EN
Partitioning of dry mass and leaf area within plants of
three species grown at elevated CO2
S. GUNN, S. J. BAILEY and J. F. FARRAR
School of Biological Sciences, University of Wales Bangor, Gwynedd LL57 2UW, UK
Summary
1. We tested the hypothesis that the net partitioning of dry mass and dry mass:area
relationships is unaltered when plants are grown at elevated atmospheric CO2 concentrations.
2. The total dry mass of Dactylis glomerata, Bellis perennis and Trifolium repens was
higher for plants in 700 compared to 350 µmol CO2 mol–1 when grown hydroponically
in controlled-environment cabinets.
3. Shoot:root ratios were higher and leaf area ratios and specific leaf areas lower in all
species grown at elevated CO2. Leaf mass ratio was higher in plants of B. perennis and
D. glomerata grown at elevated CO2.
4. Whilst these data suggest that CO2 alters the net partitioning of dry mass and dry
mass:leaf area relationships, allometric comparisons of the components of dry mass
and leaf area suggest at most a small effect of CO2. CO2 changed only two of a total of
12 allometric coefficients we calculated for the three species: ν relating shoot to root
dry mass was higher in D. glomerata, whilst ν relating leaf area to total dry mass was
lower in T. repens.
5. CO2 alone has very little effect on partitioning when the size of the plant is taken
into account.
Key-words: Allometric growth, leaf area ratio, leaf mass ratio, shoot:root ratio, specific leaf area
Functional Ecology (1999) 13 (Suppl.1), 3–11
Introduction
© 1999 British
Ecological Society
Increased atmospheric carbon dioxide concentration
usually increases plant dry mass (Patterson & Flint
1980; Baxter et al. 1994). It is less clear whether the
partitioning of dry mass and leaf area has changed.
Distribution of dry mass and leaf area is of considerable importance because it both determines future
growth (LAR and hence LWR and SLA are components
of RGR) and because the flux of C below ground is of
major significance for C sequestration (Arnone &
Körner 1995; Gifford, Lutze & Barrett 1996). Growth
at elevated CO2 may increase, decrease or not affect
the shoot:root (S:R) ratio (Patterson & Flint 1980;
Oberbauer, Strain & Fetcher 1985; Cure & Acock
1986; Koch et al. 1986; Rogers et al. 1992, 1996;
Ferris & Taylor 1993). Both SLA and LAR generally
decrease with growth at elevated CO2 (Goudriaan &
de Ruiter 1983; Oberbauer et al. 1985; du Cloux,
Daguenet & Massimino 1987; Bazzaz et al. 1989;
Newton 1991; Ferris & Taylor 1993; den Hertog,
Stulen & Lambers 1993; Pettersson, McDonald &
Stadenberg 1993) whilst LMR is unaffected (du Cloux
et al. 1987; Stulen & den Hertog 1993; Pettersson
et al. 1993). Plant development as well as growth is
faster at elevated CO2 as shown by time to flowering
(Mortensen 1987) and leaf development (Cure, Rufty
& Israel 1989). Consequently many experiments may
be measuring ontogenetic, not treatment, effects as
they involve comparing treatments at the same age of
plant.
There are three ways of separating effects of treatment from ontogeny: harvest plants at the same stage
of development, examine plants that have similar total
dry mass, and the use of allometry. In this paper we
shall concentrate on the last two methods; the former
will be addressed separately (and see Gunn, Bailey &
Farrar 1996).
It has long been recognized that in order to assess
the effect of a treatment on traits that exhibit sizedependent changes during growth, such as S:R ratios,
comparisons must be made on plants of a common size
(Evans 1972; Coleman, McConnaughay & Ackerly
1994; Coleman & McConnaughay 1995). Roumet
et al. (1996) found that LMR was unaffected by growth
at elevated CO2 whilst SLA, calculated on a total rather
than a structural leaf mass basis, was decreased.
Growth of roots and shoots are often related
through the allometric formula S = bR k, where S is
shoot dry mass, R root dry mass, and b and k are constants (Troughton 1955). Remarkably, and usefully,
3
4
Partitioning at
elevated CO2
© 1999 British
Ecological Society,
Functional Ecology,
13 (Suppl. 1), 3–11
this relationship tends to remain linear for substantial
periods of time for plant growth in an unchanging
environment, although curvilinear relationships are
also found (Pearsall 1927; Troughton 1955; Causton
& Venus 1981; Coleman et al. 1995). Although the
allometric coefficient (k) is often used to refer to the
relationship between shoot and root dry mass it can
also be used to examine relationships such as those
between leaf area and total dry mass, leaf mass and
total dry mass, and leaf area and leaf dry mass (LAR,
LMR and SLA when expressed as ratios; Coleman
et al. 1995; Barrett & Gifford 1995). A change in the
partitioning of carbon between, for example, the shoot
and the root, will be shown as a change in the value of
k. k is generally calculated by a linear regression,
using the method of least squares. However, this is not
a suitable model as there are not an independent and a
dependent variable (that is, it is as justifiable to plot
ln S as the x variable as the y variable). A better model
is the geometric mean regression or reduced major
axis (Ricker 1984).
Baxter et al. (1994) found no change in k in the relationship between shoot and root dry mass (calculated
after removal of total non-structural carbohydrates),
for Agrostis capillaris or Poa alpina due to a twofold
difference in the CO2 concentration (340 and
680 µmol CO2 mol–1). However, k is increased in
Festuca vivipara so that more dry matter is partitioned
towards the shoot than towards the root at elevated
CO2. k is unchanged in barley and Picea sitchensis at
elevated CO2 (Farrar & Williams 1991; Hibberd,
Whitbread & Farrar 1996) but decreases in Lolium
perenne (Nijs & Impens 1997). Barrett & Gifford
(1995) found that there was an increase in the allometric constant relating leaf mass and plant mass in plants
grown at elevated CO2 whilst CO2 had no effect on
the relationship between leaf area and leaf mass in
cotton. Growth CO2 concentration had no effect on
the allometric relationship between root and plant
mass in Yellow Birch (Berntson, Wayne & Bazzaz
1997).
In this study we examined the hypothesis that
growth at elevated CO2 will increase plant dry mass
but that partitioning between shoot and root, leaf area
and total dry mass, leaf mass and total dry mass, and
leaf area and leaf dry mass will be unaffected when
size and ontogeny are taken into account. Our studies
differ from others both because we compare three
ways of data presentation (ratios, and both allometry
and a procedure that scales by dry mass, as two different ways of avoiding ontogenetic effects), and because
we grew the plants so that CO2 was the only variable.
Thus the plants were grown hydroponically so that
roots had ready access to nutrients (avoiding nutrient
deficiencies that decrease S:R) and so that the water
status of the rooting medium was identical in both CO2
treatments, unlike experiments in solid media where
decreased transpiration in elevated CO2 can result in
moister soil than in the ambient treatment.
Materials and methods
PLANT GROWTH
Seeds of Trifolium repens L. cv Kent (Emorsgate
Seeds, Norfolk, UK), Dactylis glomerata L. cv Sylvan
(IGER, Aberstwyth, UK) and Bellis perennis L.
(Chiltern Seeds, Cumbria, UK) were germinated and
grown at either 350 (ambient) or 700 µmol CO2 mol–1
(elevated) in controlled-environment chambers
(Sanyo Gallenkamp PG660, Leicester, UK), at 20 °C
with a 16 h photoperiod, a photon flux density of
420 µmol m–2 s–1 at plant height, supplied by HQI
bulbs supplemented with tungsten filament bulbs and
a vapour pressure deficit of 0·7 kPa. Air was drawn
into the cabinets through a modified inlet port from a
fan (Type-3MS11, Air Control Installations, Chard,
UK) providing a flow of 60 litres min–1 which produced 5·5 complete changes of air per hour in each
cabinet. Air was enriched to 700 µmol CO2 mol–1
using CO2 supplied from vapour-withdrawal cylinders (BOC Ltd, Manchester, UK) and this concentration was controlled using an infrared gas analyser
(IRGA) to within ± 5 µmol CO2 mol–1 CO2 (EGM-1,
PP-Systems, Herts, UK).
Thirty plants were grown in 7 dm3 of solution aerated at 1 dm3 min–1. The temperature of the solution
was not controlled but was ± 1 °C of the air temperature. Solutions were changed every 3 or 4 days.
Dactylis glomerata was grown in full strength and
T. repens in half strength Long Ashton solution (mol
m–3, full strength); KNO3 (4), Ca(NO3)2. 4H2O (4),
NaH2PO4·2H2O (1·33), MgSO4·7H2O (1·5),
(0·01),
FeEDTA Na
(0·1),
MnSO4·4H2O
CuSO4·5H2O (0·001), ZnSO4·7H2O (0·001), H3BO3
(0·05), Na2MoO4·2H2O (0·004), NaCl (0·1). Sodium
metasilicate was added at the rate of 10 mg dm–3.
Bellis perennis was grown in a solution containing
(mol m–3): KNO3 (0·2) (NH4)2SO4 (0·06), Ca(NO3)2.
4H2O (0·15), KH2PO4·2H2O (0·95), K2HPO4 (0·05),
MgSO4·7H2O (0·11), Na2EDTA·2H2O (0·02),
(0·02),
MnSO4·4H2O
(0·008),
FeSO4·7H2O
CuSO4·5H2O (0·00016), ZnSO4·7H2O (0·006),
H3BO3 (0·0018), Mo7O24(NH4)6·2H2O (0·000008),
NaCl (0·02).
Plants of D. glomerata were harvested between 20
and 42 days old, B. perennis 21 and 50 days old and
T. repens 16 and 33 days old. At each harvest five
replicate plants of each species were taken randomly.
Plants of B. perennis and T. repens were divided into
leaves (excluding petioles), rest of shoot and root,
whilst those of D. glomerata were divided into (1)
main stem leaf blades which were fully expanded, (2)
rest of main stem (leaf sheaths plus expanding leaf
blades of the primary tiller plus bases of secondary
tillers), (3) tillers and (4) root. Leaf area was measured
on a leaf area meter (Delta T, type TC2014/X video
camera with electronic control unit, Cambridge, UK)
and dry mass of all parts was determined after drying
in a ventilated oven at 80 °C.
5
S. Gunn et al.
GROWTH ANALYSIS
A stepwise regression procedure was used to determine if first- or second-order polynomials were the
best fit for a natural-log transformation of shoot or
root dry mass plotted against time (days) for all plants
(Hunt 1982). t-tests were used to determine if the
quadratic term differed significantly from zero (Zar
1996), using the computer package SPSS (version 7,
SPSS, Chicago, IL, USA).
A quadratic equation best described the data for
root and shoot growth of B. perennis and all except
shoot dry mass of plants of D. glomerata grown at
ambient CO2 which was best described as a linear
regression: quadratic equations only will be shown. A
linear regression best described the data of shoot and
root dry mass of T. repens, except for roots of plants
grown at elevated CO2: linear equations only will be
shown. The first differential of the equations was used
to calculate relative growth rates. The time of the
earliest harvest was used in the quadratic equations
for D. glomerata and B. perennis.
RATIOS DESCRIBING NET PARTITIONING
LAR (leaf area/total plant dry mass, cm2 mg–1), LMR
(mass of leaves used for leaf area measurements/total
plant dry mass), S:R (shoot dry mass/root dry mass)
and SLA (leaf area/leaf mass, cm2 mg–1) were calculated for each harvest. Dry mass is the sum of both
structural and non-structural material.
Cochran’s test was used to test for the equality of variances before an analysis of variance was carried out.
Significant interactions were compared using Tukey’s
honestly significant test. Data are shown as means of
five replicates + one standard error of the mean.
To remove the effect of size, ratios were expressed
against dry mass. Discriminant function analysis (Cooper
& Weekes 1983; Tabachnick & Fidell 1996 using SPSS
statistical package) was used to assess whether it was possible to distinguish between the group of plants grown at
ambient from the group grown at elevated CO2 on the
basis of S:R ratio and total dry mass, LAR and total dry
mass, LMR and total dry mass or SLA and total dry mass
for each species. Prior to analysis the data were assessed
for the presence of outliers by Mahalanobis distance and
homogeneity of variance–covariance using Box’s M-test
(Tabachnick & Fidell 1996). Using all plants from all
harvests the variance–covariance matrices were heterogenous. After removal of plants of B. perennis and
D. glomerata with a total dry mass > 2000 mg and
T. repens > 500 mg (see Fig. 1), the variance–covariance
matrices were homogenous and discriminant analysis
was then carried out on these plants.
ALLOMETRIC COEFFICIENTS
© 1999 British
Ecological Society,
Functional Ecology,
13 (Suppl. 1), 3–11
We shall use the symbol ν with subscripts to denote
allometric coefficients calculated by geometric mean
regression; thus νSR, νAM, νLM, and νAL are the allo-
metric analogues of the ratios S:R ratio, LAR, LMR
and SLA, respectively. Allometric coefficients were
calculated for the relationships between shoot dry
mass and root dry mass (νSR), leaf area and plant dry
mass (νAM), leaf mass and plant dry mass (νLM), and
leaf area and leaf dry mass (νAL) by geometric mean
regression (Ricker 1984). In summary the natural log
of Y was plotted against the natural log of X for all
plants from all harvests. A straight line gave a better fit
than a curvilinear relationship and so the equation:
ln Y = ln a + k ln X
was then fitted through the points, where X is root, leaf
or total dry mass, Y is shoot or leaf dry mass or leaf
area, and a and k are constants. Goodness of fit of the
points to a straight line was assessed using the coefficient of determination (r2 ) (Zar 1996). The allometric
coefficient for a geometric mean regression was calculated as ν = k/r, where r is the correlation coefficient. A
comparison of the two correlation coefficients (350
and 700 µmol CO2 mol–1 within any one plot was carried out after a Fisher’s z-transformation of r (Zar
1996). Only for one plot, leaf dry mass vs total dry
mass for T. repens, was there a significant difference
between the r-values for the two lines. No allowance
for this was made in the final analysis. Comparisons of
ν were carried out using a modified t-test and results
are shown with 95% confidence limits (Ricker 1984).
Where there was no significant difference between the
slopes a comparison of the elevations (as opposed to
the intercepts) of the regressions (i.e. a comparison of
the vertical positions of the lines on the graphs) was
carried out using a t-test (Zar 1996).
Results
GROWTH
Maximum RGR ranged from 0·2 to 0·3 day–1
(Table 1). Total dry mass was higher in plants grown
at elevated compared to ambient CO2, for all three
species (values from the final harvest are shown in
Table 1). The dry mass of the shoots of T. repens,
D. glomerata and B. perennis, and the roots of
T. repens and B. perennis grown at elevated CO2 were
higher than for plants grown at ambient CO2 but
[CO2] had no effect on the root dry mass of D. glomerata (Table 1).
Total leaf area was higher in plants of B. perennis
and T. repens grown at elevated compared to ambient
CO2 (Table 1). The CO2 concentration of growth had
no effect on the total area of fully expanded leaves in
D. glomerata (Table 1).
NET PARTITIONING OF DRY MASS AND LEAF AREA
Shoot:root ratio
S:R ratio was higher in plants grown at elevated compared to ambient [CO2] in T. repens and B. perennis
6
Partitioning at
elevated CO2
Fig. 1. The effects of [CO2] on the shoot:root ratio, leaf area ratio, leaf mass ratio and specific leaf area of D. glomerata,
B. perennis and T. repens assessed on the basis of time (days). Plants were grown at either 350 (solid bars) or 700 µmol CO2
mol–1 (open bars) CO2. Values are the mean of five replicates + SE.
(P < 0·01). However, there was a significant interaction between CO2 and harvest (P < 0·05) so that only at
the final harvest was S:R ratio higher in D. glomerata
(Fig. 1).
Plants grown at ambient CO2 could be distinguished from those grown at elevated CO2 on the
basis of S:R ratio and total dry mass using discriminant function analysis for B. perennis but not D. glomerata or T. repens. On this basis the S:R ratio was
higher in B. perennis grown at elevated CO2 (Table 2).
Leaf area ratio
© 1999 British
Ecological Society,
Functional Ecology,
13 (Suppl. 1), 3–11
LAR was lower in D. glomerata (P < 0·01), B. perennis (P < 0·01) and T. repens (P < 0·001) grown at elevated compared to ambient [CO2] (Fig. 1).
Plants grown at ambient CO2 could be distinguished from those grown at elevated CO2 on the
basis of LAR and total dry mass using discriminant
function analysis for T. repens but not B. perennis or
D. glomerata. On the same criterion, LAR was lower
in T. repens grown at elevated CO2 (Table 2).
Leaf mass ratio
LMR was higher in D. glomerata (P < 0·05) and
B. perennis (P < 0·001) grown at elevated compared to
ambient CO2; LMR was unaffected by [CO2] in
T. repens (Fig. 1).
Plants grown at ambient CO2 could be distinguished from those grown at elevated CO2 on the
basis of LMR and total dry mass using discriminant
7
S. Gunn et al.
Fig. 2. The effects of [CO2] on the shoot:root ratio of D. glomerata, B. perennis and T. repens assessed on the basis of total dry
● ) CO2. Plants to the right of the vertical line are
mass (mg). Plants were grown at either 350 (●) or 700 µmol CO2 mol–1 (●
those excluded from the discriminant function analysis (see text).
function analysis for B. perennis, but not D. glomerata or T. repens. On the same criterion LMR, was
higher in B. perennis grown at elevated CO2 (Table 2).
Specific leaf area
SLA was lower in D. glomerata and T. repens
(P < 0·001) grown at elevated compared to ambient
CO2 and in B. perennis at the first harvest (Fig. 1).
Plants grown at ambient CO2 could be distinguished
from those grown at elevated CO2 in all three species
on the basis of SLA and total dry mass using discriminant function analysis. On the same criterion, SLA was
lower in plants grown at elevated CO2 (Table 2).
ALLOMETRIC COEFFICIENTS
Shoot vs root dry mass (νSR )
The allometric coefficient, νSR, relating shoot and root
dry mass was unaffected by CO2 concentration in
T. repens and B. perennis but was higher in D. glomerata grown at elevated compared to ambient CO2: there
was increased partitioning towards the shoot. There
was a significant difference between the elevations of
the regressions in B. perennis (P < 0·01) but not in T.
repens. Elevations were not compared in D. glomerata. The graphs of ln shoot dry mass vs ln root dry
mass for the three species are given in Fig. 3 as examples of allometric plots. The remaining coefficients
are given as values only (Table 3).
Leaf area vs total dry mass (νAM)
The allometric coefficient, νAM, relating leaf area to
total dry mass was unaffected by CO2 in B. perennis
and D. glomerata but was lower in T. repens grown at
elevated compared to ambient CO2 (Table 3) with less
Table 1. The effects of [CO2] on growth of T. repens, D. glomerata and B. perennis in hydroponics. Dry mass and leaf area at the final harvest.
Constants in the equations ln dry mass = a + b(time) or ln dry mass = a + b(time) + c (time)2 for shoot and root dry mass and maximum RGR (calculated
at the earliest harvest for quadratic equations). Standard errors are in brackets. NS, no significant difference
T. repens
(µmol CO2 mol–1)
D. glomerata
(µmol CO2 mol–1)
350
350
700
350
700
0·72 (0·07)
0·55 (0·05)
0·19 (0·02)
55·8 (5·3)
3·42 (0·30)
2·87 (0·28)
0·55 (0·04)
187·2 (19·2)
4·20 (0·40)
3·75 (0·40)
0·45 (0·02)
197·8 (24·8)
1·81 (0·18)
1·39 (0·15)
0·41 (0·07)
184·9 (34·4)
3·81 (0·48)
2·94 (0·35)
0·87 (0·14)
283·9 (34·7)
– 4·20 (0·57)
0·32 (0·02)
– 4·72 (1·01)
0·41 (0·07)
– 0·003 (0·001)
0·97
0·30
– 6·63 (1·40)
0·54 (0·09)
– 0·005 (0·002)
0·95
0·36 NS
– 6·22 (1·35)
0·47 (0·08)
– 0·004 (0·002)
0·93
0·30
– 3·37 (1·13)
0·35 (0·07)
– 0·003 (0·001)
0·97
0·24 NS
– 6·00 (1·49)
0·45 (0·10)
– 0·004 (0·002)
0·93
0·30
– 6·73 (1·14)
0·53 (0·08)
– 0·005 (0·001)
0·95
0·31 NS
– 7·85 (0·99)
0·49 (0·06)
– 0·004 (0·001)
0·97
0·31
– 5·33 (1·21)
0·37 (0·07)
– 0·003 (0·001)
0·97
0·26 NS
Dry mass (g)
Total
0·31 (0·06)
Shoot
0·23 (0·04)
Root
0·09 (0·02)
33·5 (5·7)
Leaf area (cm2 plant–1)
Shoot
a
– 3·14 (0·04)
b
0·26 (0·02)
c
0·94
r2
Maximum RGR (day–1) 0·26
Root
a
– 3·19 (0·38)
b
0·23 (0·02)
c
0·97
r2
Maximum RGR (day–1) 0·23
700
0·92
0·32 NS
– 4·59 (0·60)
0·31 (0·03)
0·90
0·31 NS
B. perennis
(µmol CO2 mol–1)
8
Partitioning at
elevated CO2
Table 2. The effect of [CO2] on the mean of all plants from all harvests, for the variables total plant dry mass (mg), S:R ratio,
LAR (cm2 mg–1), LMR and SLA (cm2 mg–1) in T. repens, D. glomerata and B. perennis grown in hydroponics. Prior to analysis
plants were selected on the basis of total dry mass of plants from all harvests (B. perennis and D. glomerata total dry mass
≤ 2000 mg, T. repens total dry mass ≤ 500 mg). Standard errors are shown in brackets. NS, no significant difference; *P ≤ 0·05,
**P ≤ 0·01
Dry mass
S:R ratio
LAR
LMR
SLA
T. repens
(µmol CO2 mol–1)
D. glomerata
(µmol CO2 mol–1)
B. perennis
(µmol CO2 mol–1)
350
700
350
350
93 (30)
2·0 (0·1)
0·15 (0·01)
0·39 (0·01)
0·39 (0·02)
94 (32) NS
2·2 (0·1) NS
0·11 (0·01)*
0·41 (0·03) NS
0·25 (0·01)**
618 (104)
761 (129) NS
3·8 (0·2)
4·2 (0·3) NS
0·07 (0·003) 0·06 (0·003)NS
0·22 (0·01)
0·25 (0·01)NS
0·32 (0·02)
0·26 (0·02)**
leaf area being produced per unit of total plant mass
at elevated CO2. CO2 concentration had no effect on
the elevations of the regressions in B. perennis or
D. glomerata. Elevations were not compared in
T. repens.
Leaf mass vs total dry mass (νLM)
CO2 concentration had no effect on the allometric
coefficient, νLM, relating leaf dry mass to total dry
mass in any species (Table 3). CO2 concentration had
a significant effect on the elevations of the regressions
in B. perennis and D. glomerata (P < 0·001), but not in
T. repens.
Leaf area vs leaf dry mass (νAL)
CO2 concentration had no effect on the allometric coefficient, νAL, relating leaf area to leaf dry mass in any
species (Table 3). CO2 concentration had a significant
effect on the elevations of the regressions in T. repens
(P < 0·01) but not in B. perennis or D. glomerata.
Discussion
Growth at elevated CO2 had little effect on partitioning when CO2 was the only factor varying (nutrient
© 1999 British
Ecological Society,
Functional Ecology,
13 (Suppl. 1), 3–11
700
700
608 (110)
627 (112) NS
3·1 (0·2)
3·6 (0·3)*
0·11 (0·01) 0·10 (0·01) NS
0·53 (0·01) 0·62 (0·02)*
0·22 (0·01) 0·17 (0·01)**
and water status were unaltered by CO2 treatment)
and size or ontogeny were taken into account: of the
12 relationships examined allometrically only two
were significantly affected by CO2 concentration. In
sharp contrast the conclusions that would be drawn
from a comparison of ratios at particular harvests
would be that growth at elevated CO2 resulted in
increases of the shoot:root and leaf mass ratios and
decreases of the leaf area ratio and specific leaf area
(Table 4). Such conclusions would be wrong: they are
based on a lack of appreciation of the way in which
ratios such as S:R may change with ontogeny (Farrar
& Gunn 1996).
Although any scaling procedure can be used as the
basis on which to compare treatments here we use two,
dry mass and allometry. Each has advantages and disadvantages. Only 50% of the discriminant function
analyses gave the same result as the allometric analysis
(Table 4). This apparent discrepancy may be due to the
smaller range of plants assessed when comparing
ratios on the basis of dry mass to the number used for
allometry: a better experimental procedure would be to
compare ratios from plants harvested when of similar
dry mass. The discrepency may also be due to the statistical difficulties in comparing ν between treatments
where any differences may be small and variation
large, a problem which is especially acute when using
Fig. 3. The effects of [CO2] on the allometric relationship between shoot and root dry mass of D. glomerata, B. perennis and
■ dotted line) CO2.
T. repens. Plants were grown at either 350 (■; solid line) or 700 µmol CO2 mol–1 (■
Table 3. The effect of [CO2] on the allometric coefficient relating shoot and root dry mass, leaf area and total dry mass, leaf mass and total dry mass,
and leaf area and leaf mass of T. repens, D. glomerata and B. perennis. The allometric coefficient was calculated by plotting the natural log of Y against
the natural log of X for all plants from all harvests and fitting a linear regression where X is root, leaf or total dry mass, Y is shoot or leaf dry mass or leaf
area, ln a is the intercept and k is the slope; r is the correlation coefficient. The allometric coefficient, ν, was then calculated as k/r. Values are shown
with 95% confidence limits. NS, no significant difference; *P ≤ 0·05, ***P ≤ 0·001
Shoot and root dry mass
νSR
ln a
r
Leaf area and total dry mass
νAM
ln a
r
Leaf mass and total dry mass
νLM
ln a
r
Leaf area and leaf dry mass
νAL
ln a
r
T. repens
(µmol CO2 mol–1)
D. glomerata
(µmol CO2 mol–1)
B. perennis
(µmol CO2 mol–1)
350
350
350
1·10 (0·04)
0·41 (0·08)
1·00
700
1·04 (0·05) NS
0·68 (0·08)
1·00
700
700
1·12 (0·07)
0·88 (0·11)
0·99
1·30 (0·08)***
0·43 (0·10)
0·99
0·97 (0·08)
1·30 (0·44)
0·97
0·93 (0·09) NS
1·81 (0·18)
0·97
0·93 (0·05)
– 1·66 (0·08)
0·99
0·91 (0·06)*
– 1·84 (0·09)
0·99
0·91 (0·04)
– 2·14 (0·07)
0·99
0·88 (0·05) NS
– 2·04 (0·09)
0·99
0·93 (0·05)
– 1·72 (0·09)
0·99
0·86 (0·06) NS
– 1·37 (0·09)
0·99
1·03 (0·03)
– 1·06 (0·04)
1·00
1·07 (0·06) NS
– 1·23 (0·13)
0·99
1·05 (0·04)
– 1·78 (0·06)
1·00
1·02 (0·04) NS
– 1·51 (0·07)
0·99
0·98 (0·030
– 0·55 (0·06)
1·00
0·95 (0·03) NS
– 0·24 (0·06)
1·00
0·90 (0·05)
– 0·70 (0·08)
0·99
0·89 (0·06) NS
– 0·94 (0·10)
0·99
0·86 (0·03)
– 0·60 (0·05)
1·00
0·86 (0·04) NS
– 0·76 (0·05)
1·00
0·93 (0·05)
– 1·19 (0·10)
0·99
0·89 (0·07) NS
– 1·10 (0·12)
0·98
Table 4. Summary of the effects of [CO2] on the relationships between shoot and root dry mass, leaf area and total dry mass,
leaf mass and total dry mass, and leaf area and leaf dry mass expressed as (A) ratios vs time (from Fig. 2), (B) ratios vs total dry
mass (from Table 2) and (C) allometric coefficients, ν (from Table 3). ↓, decrease; ↑, increase; NS, no significant effect of
[CO2] of growth
T. repens
Shoot and root dry mass
Leaf area and total dry mass
Leaf mass and total dry mass
Leaf area and leaf dry mass
© 1999 British
Ecological Society,
Functional Ecology,
13 (Suppl. 1), 3–11
D. glomerata
B. perennis
A
B
C
A
B
C
A
B
C
↑
↓
NS
↓
NS
↓
NS
↓
NS
↓
NS
NS
↑
↓
↑
↓
NS
NS
NS
↓
↑
NS
NS
NS
↑
↓
↑
↓
NS
NS
↑
↓
NS
NS
NS
NS
native species. Also changes in partitioning, assessed
by allometry, are determined only by changes in ν; no
account is taken of differences in the second term in
the regression equation, the intercept (ln a). For example, S:R ratios calculated from the allometric equations
relating shoot and root dry mass will be different for
treatments which differ in the value of the intercept
alone and not in the allometric coefficient. In these
experiments, however, there was generally no significant difference in the intercepts (statistical results not
shown). Overall, for these rather variable native
species, we consider allometry to be a better comparator than discriminant function analysis; not only does it
have clear biological meaning, but also, in spite of the
caveats above, it is statistically more robust.
The method used to analyse any data must be
matched to the question being asked. Allometry
answers the question—does treatment change partitioning (of area, mass, carbon, etc.)? If however, the
question relates to the relative ability of different parts
of the plant to capture resources (e.g. shoot for capturing light and root for capturing water or nutrients)
then ratios must be assessed (Farrar & Gunn 1998).
Although CO2 concentration had little effect on the
allometric coefficient, ν, it had more effect on the elevations of the regressions. Changes in elevations,
without changes in the slopes, can only have occurred
owing to early changes in the growth pattern of plants
grown at the two CO2 concentrations because common seed was used for plants grown at ambient and
elevated CO2. These early changes have never been
detected in any experiments, owing partly to the difficulties associated with measuring very small plants
and partly to the large number of replicates that would
be required to pick up such small changes in v.
Farrar & Gunn (1996) predicted that the partitioning of carbon between root and shoot should be
unchanged by growth at elevated CO2 when CO2 is
the only variable (i.e. non-limiting nutrients and
water) because there is no reason why sinks in shoots
10
Partitioning at
elevated CO2
and roots should be differentially sensitive to the
increased availability of reduced carbon. ν, relating
shoot and root dry mass, was unchanged in B. perennis and T. repens, although it was increased in plants
of D. glomerata grown at high CO2. This increase
was, however, very small and may have been due to
the differential accumulation of non-structural carbohydrates in the shoot and the root. Depending on the
question, it may be better to assess changes in partitioning on a structural dry mass basis rather than on
total dry mass because non-structural carbohydrates
may account for a significant proportion of the dry
mass of an organ (Baxter et al. 1995).
In conclusion this work has shown that it is impossible to assess the affect of a treatment on net partitioning of dry mass and area through the use of ratios
calculated at any one time. It is necessary to at least
assess the data graphically, as a plot of ratio vs total
dry mass, or allometrically. Meanwhile many conclusions in the literature must be doubted and the data
underlying the conclusions re-examined.
Acknowledgements
We would like to thank NERC for support under the
TIGER programme (section IV/1). We are grateful to
Bryan Collis for formative discussions, Peter L.
Mitchell for discussions on geometric mean regression and Louise Thurlow for technical assistance.
References
© 1999 British
Ecological Society,
Functional Ecology,
13 (Suppl. 1), 3–11
Arnone, J.A. & Körner, Ch. (1995) Soil and biomass carbon
pools in model communities of tropical plants under elevated CO2. Oecologia 104, 61–71.
Barrett, D.J. & Gifford, R.M. (1995) Photosynthetic acclimation to elevated CO2 in relation to biomass allocation
in cotton. Journal of Biogeography 22, 331–339.
Baxter, R., Ashenden, T.W., Sparks, T.H. & Farrar, J.F.
(1994) Effects of elevated carbon dioxide on three montane grass species. I. Growth and dry matter partitioning.
Journal of Experimental Botany 45, 305–315.
Baxter, R., Bell, S.A., Sparks, T.H., Ashenden, T.W. &
Farrar, J.F. (1995) Effects of elevated CO2 concentrations
on three montane grass species. III. Source leaf
metabolism and whole plant carbon partitioning. Journal
of Experimental Botany 46, 917–929.
Bazzaz, F.A., Garbutt, K., Reekie, E.G. & Williams, W.E.
(1989) Using growth analysis to interpret competition
between a C3 and a C4 annual under ambient and elevated
CO2. Oecologia 79, 223–235.
Berntson, G.M., Wayne, G.M. & Bazzaz, F.A. (1997)
Below-ground architectural and mycorrhizal responses to
elevated CO2 in Betula alleganiensis populations.
Functional Ecology 11, 684–695.
Causton, D.R. & Venus, J.C. (1981) The Biometry of
Growth. Edward Arnold, London.
du Cloux, H.C., Daguenet, M.A. & Massimino, J. (1987)
Wheat response to CO2 enrichment: growth and CO2
exchanges at two plant densities. Journal of Experimental
Botany 38, 1421–1431.
Coleman, J.S. & McConnaughay, K.D.M. (1995) A nonfunctional interpretation of a classical optimal-partitioning example. Functional Ecology 9, 951–954.
Coleman, J.S., McConnaughay, K.D.M. & Ackerly, D.D.
(1994) Interpreting phenotypic variation in plants. Trends
in Ecology and Evolution 9, 187–191.
Cooper, R.A. & Weekes, A.J. (1983) Data, Models and
Statistical Analysis. Philip Allan, Oxford.
Cure, J.D. & Acock, B. (1986) Crop responses to carbon
dioxide doubling: a literature survey. Agricultural and
Forest Meteorology 38, 127–145.
Cure, J.D., Rufty,T.W., Jr & Israel, D.W. (1989) Alterations
in soybean leaf development and photosynthesis in a CO2
enriched atmosphere. Botanical Gazette 150, 337–345.
Evans, G.C. (1972) The Quantative Analysis of Plant
Growth. University of California Press, Berkeley, CA.
Farrar, J.F. & Gunn, S. (1996) Effects of temperature and
atmospheric carbon dioxide on source–sink relations in
the context of climate change. Photoassimilate
Distribution in Plants and Crops: Source–Sink
Relationships (eds E. Zamski & A. Schaffer), pp.
389–406. Marcel Dekker, New York.
Farrar, J.F. & Gunn, S. (1998) Allocation: allometry, acclimation – and alchemy? Inherent Variation in Plant
Growth. Physiological Mechanisms and Ecological
Consequences (eds H. Lambers, H. Poorter & M. M. I.
Van Vuuren), pp. 183–198. Backhuys Publishers, Leiden.
Farrar, J.F. & Williams, M.L. (1991) The effects of increased
atmospheric carbon dioxide and temperature on carbon
partitioning, source–sink relations and respiration. Plant,
Cell and Environment 14, 819–830.
Ferris, R. & Taylor, G. (1993) Contrasting effects of elevated
CO2 on the root and shoot growth of four native herbs
commonly found in chalk grassland. New Phytologist
125, 855–866.
Gifford, R.M., Lutze, J.L. & Barrett, D. (1996) Global atmospheric change effects terrestrial carbon sequestration:
Exploration with a global C- and N-cycle model
(CQUESTN). Plant and Soil 187, 369–387.
Goudriaan, J. & de Ruiter, H.E. (1983) Plant growth in
response to CO2 enrichment, at two levels of nitrogen and
phosphorus supply. 1. Dry matter, leaf area and development. Netherland Journal of Agricultural Science 31,
157–169.
Gunn, S., Bailey, S.J. & Farrar, J.F. (1996) The effects of elevated CO2 on carbon partitioning in Dactylis glomerata.
Aspects of Applied Biology, 45. Implications of ‘Global
Environmental Change’ for Crops in Europe (eds R. J.
Froud-Williams, R. Harrington, T. J. Hocking, H. G.
Smith & T. H. Thomas), pp. 147–153. The Association of
Applied Biologists, Warwick, UK.
den Hertog, J., Stulen, I. & Lambers, H. (1993)
Assimilation, respiration and allocation of carbon in
Plantago major as affected by atmospheric CO2 levels.
Vegetatio 104/105, 369–378.
Hibberd, J.M., Whitbread, R. & Farrar, J.F. (1996) Effects of
700 ppm CO2 and infection with powdery mildew on the
growth and carbon partitioning of barley. New Phytologist
134, 309–315.
Hunt, R. (1982) Plant Growth Curves. The Functional
Approach to Plant Growth Analysis. Edward Arnold,
London.
Koch, K.E., Jones, P.H., Avigne, W.T. & Allen, L.H., Jr
(1986) Growth, dry matter partitioning, and diurnal activities of RuBP carboxylase in citrus seedlings maintained
at two levels of CO2. Physiologia Plantarum 67,
477–484.
Mortensen, L.M. (1987) Review: CO2 enrichment in greenhouses. Crop responses. Scientia Horticulturae 33, 1–25.
Newton, P.C.D. (1991) Direct effects of increasing carbon
dioxide on pasture plants and communities. New Zealand
Journal of Agricultural Research 34, 1–24.
Nijs, I. & Impens, I. (1997) An analysis of the balance
11
S. Gunn et al.
© 1999 British
Ecological Society,
Functional Ecology,
13 (Suppl. 1), 3–11
between root and shoot activity in Lolium perenne cv.
Melvina. Effects of CO2 concentration and air temperature. New Phytologist 135, 81–91.
Oberbauer, S.F., Strain, B.R. & Fetcher, N. (1985). Effect of
CO2-enrichment on seedling physiology and growth of
two tropical tree species. Physiologia Plantarum 65,
352–356.
Pattersson, D.T. & Flint, E.P. (1980) Potential effects of
global atmospheric CO2 enrichment on the growth and
competitiveness of C3 and C4 weed and crop plants. Weed
Science 28, 71–75.
Pearsall, W.H. (1927) Growth studies. VI. On the relative
sizes of growing plant organs. Annals of Botany 151,
549–556.
Pettersson, R., McDonald, A.J.S. & Stadenberg, I. (1993)
Response of small birch plants (Betula pendula Roth.) to
elevated CO2 and nitrogen supply. Plant, Cell and
Environment 16, 1115–1121.
Ricker, W.E. (1984) Computation and uses of central trend
lines. Canadian Journal of Zoology 62, 1897–1905.
Rogers, H.H., Peterson, C.M., McCrimmon, J.N. & Cure,
J.D. (1992) Response of plant roots to elevated atmospheric carbon dioxide. Plant, Cell and Environment 15,
749–752.
Rogers, H.H., Prior, S.A., Runion, G.B. & Mitchell, R.J.
(1996). Root and shoot ratio of crops as influenced by
CO2. Plant and Soil 187, 229–248.
Roumet, C., Bell, M.P., Sonie, L., Jardon, F. & Roy, J. (1996)
Growth response of grasses to elevated CO2: a physiological plurispecific analysis. New Phytologist 133,
595–603.
Stulen, I. & den Hertog, J. (1993) Root growth and functioning under atmospheric CO2 enrichment. Vegetatio
104/105, 99–115.
Tabachnick, B.G. & Fidell, L.S. (1996) Using Multivariate
Statistics. Harper Collins, NY, USA.
Troughton, A. (1955) The application of the allometric formula to the study of the relationship between the roots and
shoots of young grass plants. Agricultural Progress 30,
59–65.
Zar, J.H. (1996) Biostatistical Analysis. Prentice Hall Inc,
New Jersey.