Annals of Botany 77 : 35–45, 1996
Radiation Interception, Partitioning and Use in Grass–Clover Mixtures
O. F A U R I E*, J. F. S O U S S A N A* and H. S I N O Q U ET†
* Fonctionnement et Gestion de l’Ecosyste[ me Prairial, INRA-Agronomie. 12 AŠ. du BreU zet, and
† PIAF, INRA-Bioclimatologie, Domaine de Crouelle, 63039 Clermont-Ferrand Cedex 2, France
Received : 24 May 1995
Accepted : 29 August 1995
Mixed swards of perennial ryegrass}white clover were grown in competition under controlled environmental
conditions, at two temperatures and with different inorganic nitrogen supplies. The swards were studied after canopy
closure, from 800 to 1200 °C d cumulative temperatures. Clover contents did not vary significantly during the period.
A simulation model of light interception was used to calculate light partitioning coefficients and radiation use
efficiencies for both components of the mixture in this controlled environment experiment. Additionally, this same
radiative transfer model was applied to the field data from Woledge (1988) (Annals of Applied Biology 112 : 175–186)
and from Woledge, Davidson and Dennis (1992) (Grass and Forage Science 47 : 230–238). The measured and
simulated values of light transmission, at different depths in the mixed canopy, were highly correlated (P ! 0±001)
with more than 80 % of the total variance explained. The daily average of photosynthetically active radiation (PAR)
interception in a natural environment was estimated from simulations, for the field and controlled environment data.
Under these conditions, white clover captured significantly more light per unit leaf area than perennial ryegrass at low,
but not at high, nitrogen supply.
In the controlled environment experiment, the radiation use efficiency of the legume was lower than that of its
companion grass. For both species, radiation use efficiency was negatively correlated with the mean irradiance of the
leaf. The role of a compensation between light interception and light use for stabilizing the botanical composition of
dense grass–clover swards is discussed.
# 1996 Annals of Botany Company
Key words : Light interception, radiation transfer model, growth analysis, radiation use efficiency, grassland, white
clover, perennial ryegrass, Trifolium repens L., Lolium perenne L.
INTRODUCTION
Temperate perennial grasses and legumes differ with respect
to radiation interception and conversion efficiencies. In
monocultures, light is fully intercepted at a lower leaf area
index with legumes than with grasses (Brougham, 1958) ; on
the other hand, the radiation use efficiency of C grasses
$
tends to be higher than that of legumes (Gosse et al., 1986).
Competition for light is considered to be important in
determining whether grass or legumes dominate in mixed
swards (Haynes, 1980). With perennial ryegrass (Lolium
perenne L.) and white clover (Trifolium repens L.) mixtures,
long regrowth periods in conditions more favourable to
grass growth (low temperatures, high availability of mineral
nitrogen) lead to strong competition for light and quite
often to a decline in the proportion of clover (Frame and
Newbould, 1986).
White clover has a greater proportion of its leaf lamina in
the upper, well lit, layers of the canopy than grass (Dennis
and Woledge, 1985 ; Woledge, 1988 ; Woledge et al., 1992).
It seems therefore unlikely, even in nitrogen fertilized
mixtures (Woledge, 1988), that the enhancement of grass
growth could cause it to overtop and shade the clover. Yet,
in nitrogen fertilized permanent grasslands, the small
proportion of white clover was thought to be due to the
large leaf area of the other species at heights which white
clover could not attain (Schwank, Blum and No$ sberger,
1986). However, in these reports, no attempt was made to
0305-7364}96}010035­11 $12.00}0
calculate light partitioning between grass and clover and
thus to compare their light interception efficiencies in the
mixed canopy.
White clover leaves have high photosynthetic capacities
(Woledge, Dennis and Davidson, 1984 ; Dennis and
Woledge, 1985) and even in situ in the sward, where grass
was dominant (nitrogen fertilized plots), clover laminae had
a greater assimilation rate of "%CO per unit leaf area than
#
grass (Woledge, 1988). This was also reported for simulated
mixed swards grown in a controlled environment (Davidson
and Robson, 1985).
The balance between species within the mixed sward
depends upon the relative growth rate of each component
(Woledge, 1988). The net assimilation rate of the leaf
surface is not the only factor determining the plant relative
growth rate ; respiratory losses (Haystead et al., 1980 ; Ryle,
Arnott and Powell, 1981) and biomass partitioning between
organs (Ko$ rner, 1990) can be of overwhelming importance.
As a result, clover radiation use efficiency may be lower, in
mixed swards, than that of the grass. Yet, there is little
evidence of a lower radiation use efficiency of the legume in
a mixed sward. Models of radiation interception are needed
to calculate the efficiencies of photosynthetically active
radiation (PAR) capture and of PAR use for species grown
in mixture. By using such a model, Sinoquet et al. (1990)
calculated that the radiation use efficiency of white clover
was lower than that of the tall fescue in a nitrogen-fertilized
mixture. However, some simplifications were made : (a) the
# 1996 Annals of Botany Company
36
Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards
canopy was only one horizontal layer, which did not
account for differences in the vertical distribution of leaf
area between grass and clover ; (b) leaf lamina angles were
assumed to be constant. Moreover, as with most field
studies, the radiation use efficiency was presumably underestimated as the root biomass was not taken into account
(Russell, 1993).
In the present study, a similar light model, but using
several horizontal layers of leaves, was applied to the field
data reported by Woledge (1988) and by Woledge et al.
(1992) and to results from a controlled environment
experiment with mixed grass-clover swards. Light partitioning was calculated and, for the controlled environment
experiment, a growth analysis technique based on the whole
plant growth rate, allowed separate calculation of grass and
clover radiation use efficiencies.
MATERIALS AND METHODS
Radiation interception model
The simulation model of radiation interception computes
the terms of the radiation balance of horizontally homogeneous, mixed crops. Most details of the model have been
previously given (Sinoquet et al., 1990), thus only the main
features are summarized here. The model is based on the
turbid medium analogy (see Ross, 1981). In the version used
in the present study, the canopy is divided into horizontal
layers containing foliage of either a single or the two species.
Each layer is characterized by the leaf area index (LAI),
mean inclination and leaf scattering coefficient of each
species present in the layer. Other model inputs are the sun
elevation, the direct and diffuse radiation at the top of the
canopy, and the soil reflectance. Radiation interception for
each sky direction is computed from Beer’s law adapted to
partition light between species in mixed layers (Sinoquet
and Bonhomme, 1991). This is used to derive interception of
direct radiation (i.e. coming from a single sun direction)
and diffuse light (i.e. assumed to come from a finite set of
sky directions). Scattering is characterized by exchange
coefficients between each pair of vegetation layers, which
combines scattering on leaf surfaces, assumed to be
lambertian, and interception of scattered radiation. The
radiation balance of the canopy, i.e. coupling between
interception and multiple scattering is solved using a method
similar to the ‘ radiosity ’ method (Ozisik, 1981). This
consists of expressing the radiation fluxes intercepted by
each component (i.e. each species foliage in each vegetation
layer) as a linear combination of the fluxes coming from the
radiation sources : (a) direct and diffuse incident radiation
weighed by the interception probabilities ; (b) fluxes scattered
by the canopy components weighed by the above exchange
coefficients. This makes a system of linear equations where
intercepted fluxes are the unknown and which is iteratively
solved (Sinoquet and Bonhomme, 1992). Radiation transmitted below each vegetation layer and absorbed by each
species in each layer is thus computed. Because of changes
in optical properties of leaf and soil surface, a simulation
has to be run for each waveband. The solar spectrum is split
into two domains—PAR (400–700 nm) and near infra-red
(NIR, above 700 nm)—in which optical properties are
assumed to be constant and incident radiation equally
distributed (50 % in each band, Varlet-Grancher, 1975,
amongst others). In this study, leaf transmittance was
assumed to be 0±10 for both grass and legume species in the
PAR band, and 0±47 and 0±49 in the NIR band for tall fescue
and white clover, respectively (Nijs and Impens, 1993 ;
Varlet-Grancher, pers. comm.).
Controlled enŠironment experiment
Plant cultiŠation. Seeds of white clover (Trifolium repens
L., cv. Grasslands Huı$ a) and perennial ryegrass (Lolium
perenne L., cv. Pre! fe! rence) were germinated in the dark at
20 °C. After 3 d, the seedlings were transferred to an aerated
basal nutrient solution (Faurie and Soussana, 1993) and
grown in a controlled environment cabinet at 500 µmol
PAR m−# s−" with a 14-h photoperiod at 20}16 °C, day}night
temperature, respectively. Ten days after sowing, the clover
seedlings were inoculated with Rhizobium leguminosarum
bv. trifolii USDA 2063. One week later, simulated grass–
clover swards were made by transplanting 21 plants of each
species (in six alternate grass–clover rows) to a container
(0±40¬0±60) m# surrounded with reflective side panels. For
each species, five development classes were made, according
to the leaf number and to the leaf length, and plants from
the two medium classes were distributed at random among
the replicate containers. After transplantation, the simulated
mixed swards were grown, under the same conditions, either
at (20}16) °C (T­) or at (12}9) °C (T®) day}night
temperature, until a cumulative temperature sum of 1200 °C
d was reached, 65 (T­) or 100 (T®) d after sowing. The
swards were rotated twice weekly around the growth cabinet.
Two successive experiments were carried in the same growth
cabinet, one at T­ and one at T®.
The basal liquid medium was renewed twice weekly and
supplemented every 2 d with Ca(NO ) . Two amounts of N
$#
supply (N®, N­) were compared at the two temperatures
(T®, T­). A total of 50 and 200 mg N-NO− per plant at
$
N® and N­, respectively, was supplied to the mixed
swards during their growth after transplantation. As nitrate
supply was based on the thermal time, the amounts supplied
every 2 d were smaller at T® than T­.
To avoid inhibition of clover N fixation by excess nitrate
#
(Faurie and Soussana, 1993), nitrate supply was adjusted to
the mean growth rate of the mixed sward, determined in
preliminary experiments (Faurie, 1994). Thus, NO− supply
$
varied from 0±82 to 170 (N®) or from 3±3 to 710 (N­) µg
−
−
N-NO °C d " per plant. This N supply mode, derived
$
from the relative addition technique (Ingestad, 1982), was
compared, at T­, to a constant N supply of 56 (N®) or 225
(N­) µg N-NO− °C d−" per plant, resulting in the same
$
total N supply over the growth period.
Canopy structure, growth analysis and radiatiŠe balance
simulation. After canopy closure, from approx. 800 to
1200 °C d cumulative temperature sums—that is from 38 to
65 (T­) or from 64 to 100 (T®) d after sowing—sward
measurements were carried out on four occasions, approximately weekly. At each harvest, one simulated sward per
treatment was taken at random. Light (photosynthetic
Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards
37
T     1. Mean total sward biomass, mean percentage cloŠer content in total biomass and in leaf area in simulated mixed
swards after canopy closure, at the beginning (800 °C d after sowing) and at the end (1200 °C d) of the controlled enŠironment
experiment
T®
Total sward
biomass (g d. wt m−#)
Clover content in
total biomass (%)
Clover content in
leaf area (%)
ANOVA
Factor
N supply
N supply mode
Factor
Thermal time
Temperature
N®
N­
Thermal time (°C d)
RA
RA
C
RA
C
RA
800
1200
800
1200
800
1200
330
980
24
23
33
33
610
1440
11
14
13
20
300
840
49
59
56
66
270
720
69
75
76
78
330
900
51
46
52
36
290
870
53
49
57
48
Total sward biomass
T®
*
—
N®
**
NS
T­
T­
**
*
N­
**
*
N®
Clover content in total biomass
T®
*
—
N®
NS
**
T­
*
*
N­
NS
**
N­
Clover content in leaf area
T®
*
—
N®
NS
**
T­
**
*
N­
NS
*
(T®), (T­), temperature ; (N®), (N­), N supply ; (C), (RA), constant or relative addition of N (see Materials and Methods). (*, **) denote,
respectively, a significant (P ! 0±05) and a highly significant (P ! 0±01) effect (ANOVA). The effects of the N supply and of the N supply mode
were tested by ANOVA for each temperature. The effects of the thermal time and of the temperature were tested by ANOVA for each N supply
with the relative addition N supply mode.
photon flux) extinction profile was measured using a sunfleck
ceptometer (Decagon Devices Inc, Pullman, WA, USA)
placed at different depths within the canopy (every 2 or
3±5 cm at the top and thereafter every 7 cm), hence delimiting
horizontal canopy layers. Canopy geometrical structure was
then described for each of these horizontal layers. First,
clover and grass leaf lamina angles were recorded (30
replicates each). The plastic sheet supporting the sward was
then turned upside down and the whole canopy layer
clipped with battery powered shearers. The cut material was
separated into grass and clover and subsamples taken. The
grass subsample was separated into leaf lamina, sheath and
dead material and clover into leaf lamina, petiole, stolon
and dead material. The lamina area was measured (LI-3100,
Area Meter, Li-Cor, Lincoln, Nebraska, USA). Finally
roots were also harvested and separated to grass and clover.
For each layer, all fractions of the subsamples and the
remainder of grass and clover were dried at 80 °C for 24 h
and weighed. The amount of dead material in the total
sward mass was always less than 10 %. The simulations of
the radiative balance were made, assuming a vertical light
source and 10 % of diffuse radiation in the PAR waveband,
the conditions in the growth cabinet.
Field data analysis : radiatiŠe balance simulation
Woledge (1988) and Woledge et al. (1992) determined the
canopy structure of mixed tall fescue}white clover swards or
mixed ryegrass}clover swards, using the point quadrat
technique (Warren-Wilson, 1959, 1963) and calculated the
vertical distribution of foliage area for both species. These
data were used as inputs for the radiative transfer model.
Since no measurements of leaf laminae angles were reported,
we assumed (a) a clover leaf lamina angle of 25°, as this
mean value was found to be constant over a wide range of
growth conditions in the controlled environment study ; (b)
that, for a given canopy height and for a given layer height,
grass leaf blade angles were similar to those obtained in the
controlled environment study.
Tube solarimeters (measuring radiation in the
400–2500 nm waveband) were used in the field studies by
Woledge (1988) and Woledge et al. (1992), to determine
daily averages of the light extinction profile. The radiative
transfer simulations were run by assuming 100 % diffuse
radiation, since such conditions usually yield estimates of
radiative balance that are close to the daily averages (VarletGrancher and Bonhomme, 1979 ; Sinoquet et al., 1990 ;
Sinoquet and Bonhomme, 1992).
RESULTS
Sward productiŠity and cloŠer content in the controlled
enŠironment experiment
At the time of canopy closure, approximately 800 °C d
cumulative temperature, the percentage clover contents of
the simulated swards differed markedly (Table 1). The mean
clover content, both in biomass and in leaf area, was
significantly lower at T® (9}12) °C than at T­ (20}16) °C
38
Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards
A Ryegrass
Clover
B Ryegrass
Clover
C Ryegrass
Clover
Height (cm)
40
30
20
10
N–T+RA
LAI=1.1
N–T–RA
LAI=2.0
N–T+C
LAI=1.5
0
D Ryegrass
Clover
E Ryegrass
Clover
F Ryegrass
Clover
Height (cm)
40
30
20
10
N+T+RA
LAI=1.1
N+T–RA
LAI=5.4
0
60
40
20
0
G Ryegrass
20
40
Clover
60 60
40
N+T+C
LAI=1.4
20
0
H Ryegrass
20
40
Clover
60 60
40
20
0
I Ryegrass
20
40
60
Clover
Height (cm)
40
30
20
10
N–T+RA
LAI=9.2
N–T–RA
LAI=8.3
N–T+C
LAI=9.1
0
J Ryegrass
Clover
K Ryegrass
Clover
L Ryegrass
Clover
Height (cm)
40
30
20
10
N+T+RA
LAI=11.2
N+T–RA
LAI=12.9
0
60
40
20
20
0
(m2m–3)
40
60 60
40
20
N+T+C
LAI=10.9
0
20
(m2m–3)
40
60 60
40
20
0
20
(m2m–3)
40
60
F. 1. Vertical distribution of ryegrass and white clover leaf area density after 800 (A to F) and 1200 (G to L) °C d thermal time (T®), (T­),
respectively, 12}9 °C and 20}16 °C ; (N®), (N­), respectively, low and high N supply, (C), (RA), respectively, constant and relative addition N
supply mode. The treatment (N supply, temperature, N supply mode) and the sward LAI are mentioned at the bottom of each figure. The dotted
line separates the upper layers of the canopy (cumulative LAI below 3).
Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards
40
60°
30
30°
25
0°
A
80
Calculated (%)
Layer height (cm)
35
100
90°
39
20
15
60
40
20
10
5
100
15
20
25
35
30
Sward height (cm)
B
40
F. 2. Mean leaf lamina angle of grass within horizontal layers of a
simulated ryegrass-white clover canopy as a function of sward height (x
axis) and of layer height (y axis). The mean leaf lamina angle is shown
as the angle (in °) of a line segment. An angular scale, graduated in °,
is given for comparison. The results are the means of two to five canopy
layers, with 30 replicate measurements per layer.
and at N­ compared to N®, with no significant interactions
between the factors (Table 1). The clover contents which
were established at the time of canopy closure did not vary
significantly during competitive growth (Table 1). For the
same temperature sum, the total biomass of the sward was
significantly (P ! 0±01) lower at T­ than at T®, presumably due to the smaller amount of radiation accumulated
at T­ (shorter growth period) (Table 1).
Two N supply modes (either constant or according to the
relative addition technique) were compared at T­
(20}16 °C). With the constant nitrogen supply mode, the
total sward biomass was greater, but the proportion of
clover in the sward, both in terms of total biomass and of
leaf area, was significantly smaller (Table 1).
Canopy structure in the controlled enŠironment experiment
The stratified clipping technique allowed us to plot the
vertical distribution of leaf area density for the mixed
swards of grass and clover, at the start (800 °C d) and at the
end of the experiment (1200 °C d) (Fig. 1). At a given
thermal time, perennial ryegrass developed a larger total
leaf area at T® than at T­ and with N­ than with N®
(Fig. 1).
At the end of the experiment, the mixtures formed dense
canopies, with LAI between 8±3 and 12±9. For each species,
the vertical distribution of leaf area was then of overwhelming importance for PAR interception. A large N
supply increased the mean height of the canopy from 30 to
approx. 40 cm (Fig. 1). With N®, clover leaf area density in
the upper canopy layers was usually larger than that of the
grass. However, the opposite occurred at N­, especially as
ryegrass leaf area density was greatest in the first centimetres
of the mixed canopy (Fig. 1). Low temperatures (T®)
reduced clover leaf area density, both in the lower and in the
upper layers of the mixed canopy, whereas ryegrass leaf area
80
Calculated (%)
0
60
40
20
0
20
40
60
Measured (%)
80
100
F. 3. Comparison between simulated and calculated transmitted
radiation using : (A) ceptometer (in the PAR waveband) for controlled
environment study (10 % diffuse radiation) ; (B) tube solarimeters (in
the 400–2500 nm waveband) in the field studies by Woledge, 1988 and
Woledge et al., 1992 (100 % diffuse radiation). Horizontal layers from
the top : (E) 1, (D) 2, (+) 3, (*) 4, (_) 5, (^) 6, (y) 7, (x) 8 and (U)
9. The equations of the regressions plotted in (A) and (B) are,
respectively, [y ¯ (0±85³0±03)x, r ¯ 0±91, n ¯ 77, P ! 0±001] and [y ¯
(0±92³0±04)x­(3±1³2±5), r ¯ 0±92, n ¯ 100, P ! 0±001]. The dashed
lines show the confidence interval of the regression at P " 0±95.
density was enhanced (Fig. 1). As a result, the environmental
conditions that favoured grass growth in leaf area (N­,
T®) also promoted its vertical dominance relative to the
legume.
The mean angle of ryegrass leaf blade was calculated for
horizontal layers at different depths and according to the
mean sward height (Fig. 2). For a given sward height, the
decrease in the mean leaf blade angle with height in the
canopy reflects the curvature of grass leaves. This curvature
increased with leaf length and therefore with canopy height
(Fig. 2). Thus, the tall canopies formed at N­ were partly
constituted, in the upper layers, by rather horizontal grass
leaves (Fig. 2) with a large leaf area density (Fig. 1).
Partial Šalidation of the radiatiŠe balance simulations
The simulation results of transmitted radiation, below
each vegetation layer, were compared with the light
extinction profiles measured in the controlled environment
study, and tube solarimeters in the field studies by Woledge
(1988) and Woledge et al. (1992) (Fig. 3). The percentage
Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards
100
% LAI grass
A
100
100
% PAR capture clover
Calculated (%)
80
60
40
T–
20
T+
0
100
B
80
60
40
20
0
0
A
80
20
60
40
d
c
40
60
b
a
20
80
0
20
40
60
% LAI clover
100
80
60
80
100
20
0
% PAR capture grass
40
100
% LAI grass
100
40
20
0
2
4
6
8
10
Cumulative LAI
12
14
F. 4. Calculated values of transmitted radiation as a function of
cumulative leaf area from the top of the sward to the height of the
layer : (A) in controlled environment study (10 % diffuse radiation) and
(B) in the field studies (Woledge, 1988 ; Woledge et al., 1992) (100 %
diffuse radiation). Horizontal layers from the top : (E) 1, (D) 2, (+) 3,
(*) 4, (_) 5, (^) 6, (y) 7, (x) 8 and (U) 9. The equations of the
regressions plotted in (A) and in (B) are, respectively, (y ¯ 100
exp(−!±%&³!±!#)x, r ¯ 0±99, n ¯ 34, P ! 0±001 at T® and y ¯ 100
exp(−!±'*³!±!")x, r ¯ 0±99, n ¯ 48, P ! 0±001 at T­) and (y ¯ 100
exp(−!±%!*³!±!!%)x, r ¯ 0±99, n ¯ 112, P ! 0±001). The dashed lines show
the confidence interval of the regression at P " 0±95.
transmitted global radiation (field data), or transmitted
PAR (controlled environment experiment), show that the
simulated and measured values are highly correlated (P !
0±001) and that the model accounts for more than 80 % of
the total variance. The linear regression does not differ
significantly from the 1 : 1 slope for the field study.
Nevertheless, in the controlled environment study, the slope
of the linear regression is significantly less than one (Fig.
3 A).
Simulated values of the percentage transmitted radiation
are plotted in Fig. 4, as a function of the cumulative leaf
area from the sward surface. The simulation results in a
clear exponential decline in the percentage transmitted
radiation (Fig. 4 A and B). In the controlled environment
experiment the decline in the percentage transmitted
radiation was faster at T­, compared to T® (Fig. 4 A). The
planophile foliage of clover led to greater light extinction in
the upper layers, with the vertical light source of the growth
cabinet. The higher clover content in leaf area at T­
40
0
B
80
20
d
60
c
40
40
b
a
60
20
0
80
20
40
60
% LAI clover
80
100
% PAR capture grass
60
% PAR capture clover
Calculated (%)
80
100
F. 5. Species content in leaf area and contribution to the sward PAR
capture : (A) in the field studies (E) N® (Woledge, 1988), (D) N­
(Woledge, 1988), (_) N® (Woledge et al., 1992) ; (B) in the controlled
environment study. (E) N® T­, (D) N­ T­, (+) N® T®, (*)
N­ T®. The dashed lines show different values (a, b, c, d) of the ratio
of clover to grass PAR capture per unit leaf area : 1±5 (a), 2±3 (b), 3±4 (c),
5±1 (d).
therefore decreased the percentage transmitted radiation at
a given LAI.
Light partitioning between grass and cloŠer
Under field conditions. For the field data of Woledge
(1988) and Woledge et al. (1992), the simulation of radiative
transfer shows that, in a mixture, clover captured a
significantly (Wilcoxon sign-test, P ! 0±001) larger proportion of the light than its contribution to the mixed sward
LAI (Fig. 5 A). Hence, clover captured relatively more PAR
per unit leaf area than grass.
To quantify this difference, constant values of the clover
to grass ratio of PAR capture per unit leaf area are shown
by dashed lines in Fig. 5. In comparison with these constant
ratios, it appears that in mixtures with a large clover content
(more than 45 % of the total leaf area), clover laminae
usually captured two to three times more PAR per unit leaf
area than grass. By contrast, in mixtures with a lower clover
Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards
(Sinoquet et al., 1990), the legume radiation use efficiency
(RUE) was significantly smaller (Student’s t-test, P ! 0±001)
than that of ryegrass (Fig. 6). For both species, the radiation
use efficiency declined exponentially (mono-exponential
plus residual model, P ! 0±01, r ¯ 0±490) with the mean
PAR capture per unit leaf area (Fig. 6 A). Thus, clover’s
lower RUE was apparently related to the larger mean
amount of PAR captured, per unit area, by its leaf laminae.
As the lower canopy layers are shaded, they contribute little
to the PAR conversion. Thus, the same correlation was
tested by using the mean amount of PAR captured per unit
leaf area in the upper canopy layers, that is in canopy layers
with a cumulative LAI below 3. The same mono-exponential
plus residual model was highly significant (P ! 0±001, r ¯
0±601) (Fig. 6 B).
A
3.0
RUE (gDW mol–1 photon)
41
2.5
2.0
1.5
1.0
0.5
0
B
RUE (gDW mol–1 photon)
3.0
Growth rate
2.5
In the controlled environment experiment, due to its
lower radiation use efficiency, the contribution of clover to
the growth (estimated as the mean growth rate of whole
plants) of the mixed sward was smaller (Wilcoxon’s signtest, P ! 0±001) than its contribution to the PAR capture by
the mixture (Fig. 7 A). However, clover contributed to the
mixed sward growth in proportion to its contribution to the
mixed sward leaf area index and total biomass (Fig. 7 B and
C).
2.0
1.5
1.0
0.5
0
40
80
120
160
200
240
DISCUSSION
(µ mol photon m–2 s–1)
F. 6. Radiation use efficiency (RUE) as a function of the mean
amount of radiation absorbed per unit leaf area in the controlled
environment : (A) in total leaf area ; (B) in the upper layers of canopy
(cumulative LAI below 3). Solid symbols, ryegrass ; open symbols,
white clover. (E, D) N® T­, (y, x) N­ T­, (+, *) N® T®, (_,
^) N­ T®. The equations of the regressions plotted in (A) and (B)
are, respectively, [y ¯ (2±9³0±3) exp(−!±!!%)³!±!!"%)x, r ¯ 0±490, n ¯ 32,
P ! 0±01] and [y ¯ (3±9³0±1) exp(−!±!!(&³!±!!"&)x, r ¯ 0±601, n ¯ 32,
P ! 0±001]. The dashed lines show the confidence interval of the
regression at P " 0±95.
content (less than 40 % of the total leaf area) clover laminae
were somewhat less favoured, as they captured about 50 %
more radiation per unit area than grass laminae (Fig. 5 A).
Under controlled enŠironment conditions. In the controlled
environment experiment, the simulation of radiation interception was run with a vertical light and 10 % diffuse
radiation. As for the field data, clover captured a greater
proportion of the PAR (significant, Wilcoxon’s sign-test,
P ! 0±001) than its contribution to the LAI of the mixed
sward (Fig. 5 B). Clover laminae captured, at N® and N­,
respectively, (2±5³0±2) and (1±6³0±2) times more radiation
per unit leaf area than grass (Fig. 5 B). The advantage of
clover in terms of radiation interception was therefore
greater at the low N supply.
Radiation use efficiency
In the controlled environment experiment, radiation use
efficiencies of clover and grass were compared. In agreement
with previous conclusions from monocultures and mixtures
Model Šalidity
The hypothesis of considering the mixture as a horizontally
homogeneous, well mixed canopy is not too unrealistic :
first, clover has a stoloniferous growth habit resulting in
horizontal homogenization ; second the grass, albeit sown in
rows, rapidly increased its leaf area, thus colonizing the
space between the rows.
Discrepancies between measured and modelled values of
transmitted radiation (Fig. 3) may be due to both
measurement and model features. First of all, data scattering
may be related to the strictness of the model-measurement
comparison which applied to thin vegetation layers (from 2
to 7 cm). Classical validation of light models is based on
radiation transmitted on the soil surface or vertical profiles
of downward radiation only in the case of tall canopies.
Model testing from the radiation balance of small vegetation
layers involves greater uncertainty about the description of
canopy structure and in light measurements. Both are
subject to errors in identifying the layer boundaries (i.e.,
stratified-clipping method, sensor location). Turning the
growth cabinet sward to clip makes the stratified harvest
easier but probably modifies the vertical profile of leaf area,
due to upside down gravity. Light measurements within the
canopy also disturb canopy structure by parting the foliage :
this allows more radiation to fall on the sensor and
overestimates transmittance. This phenomenon is undoubtedly enhanced in our study because of the dense sward
canopy and the vertical incident light.
However, model features may also explain some deviations. The canopy is assumed to be horizontally homo-
Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards
% PAR capture grass
100
80
60
40
20
0
100
80
60
40
20
0
100
80
20
80
20
60
40
60
40
40
60
40
60
20
80
20
80
0
20
40
60
80
% PAR capture clover
100
% dDW clover
0
A
% dDW grass
% dDW clover
100
% LAI grass
100
0
B
0
20
40
60
% LAI clover
80
100
% dDW grass
42
100
Grass content (%)
% dDW clover
100
80
60
40
20
0
0
C
80
20
60
40
40
60
20
80
0
20
40
60
Clover content (%)
80
100
% dDW grass
100
100
F. 7. Species contribution to the mixed sward growth (dDW) in the controlled environment as a function of clover content in (A) PAR capture,
(B) leaf area and (C) total biomass. (E) N® T­, (D) N­ T­, (+) N® T®, (*) N­ T®.
geneous although it was sown in alternate rows. Even if the
whole canopy seems to be horizontally homogeneous after
canopy closure, effects of the row planting pattern may
persist : non-uniform distribution of leaf area of each species
in the horizontal plane may occur. A simulation study made
from a light model devoted to row intercropping showed
that such horizontal heterogeneity leads to a slight increase
in light penetration (­0±02 at total LAI ¯ 4) when the two
species have contrasted leaf inclination (i.e. planophile Šs.
erectophile) and most radiation comes from vertical directions (Sinoquet and Bonhomme, 1992). This effect is not
large enough to explain the overestimation by the whole
model found in the growth cabinet experiment. Moreover,
the same simulation study showed that the row effect does
not modify light transmission in the case of overcast sky.
This may be related to the unbiased relationship found with
the Woledge’s data set where daily transmittances are
computed by assuming an overcast sky. Ultimately these
results suggest that : (a) neglecting the row structure in the
growth cabinet experiment does not significantly bias the
transmittance calculations ; (b) the horizontally homogeneous canopy associated with overcast sky conditions
leads to a satisfactory simulation of the daily radiative
balance of the grass–legume mixture.
Such model-measurement comparison is unable to test
the model’s ability to partition light capture between the
two components. This is a crucial problem because radiation
models for intercropping are usually aimed at estimating
light competition in mixtures. In this study, the row effect
on associated vertical incident light in the growth cabinet
could have modified significantly light partitioning by
counterbalancing the effect of overtoping of the dominant
species. On the other hand, at the daily scale, simulations
have shown that the row structure of the canopy does not
significantly change light partitioning in the case of either
clear or overcast sky (Sinoquet and Bonhomme, 1992).
Light partitioning
Results from the radiative transfer model show that
clover captured more PAR than grass per unit leaf area,
both under field and under controlled environment conditions (Fig. 5). Yet, in the controlled environment
experiment, the growth conditions clearly favoured PAR
Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards
% LAI grass
40
20
0
100
80
20
60
40
40
60
20
80
0
100
0
20
40
60
% LAI clover
80
100
100
80
60
40
20
0
0
B
80
20
60
40
40
60
20
80
0
20
40
60
% LAI clover
80
100
% PAR capture grass
60
A
% PAR capture clover
% PAR capture clover
80
% LAI grass
% PAR capture grass
100
100
43
100
% LAI3 grass
% PAR capture clover
100
80
60
40
20
0
0
C
80
20
60
40
40
60
20
80
0
20
40
60
% LAI3 clover
80
100
% PAR capture grass
100
100
F. 8. Species content in leaf area and contribution to the sward PAR capture calculated with (A) the complete light model or (B) modified model,
assuming the same leaf lamina angle for grass and clover (see discussion). (C) Species content in leaf area and contribution to the total PAR in
the upper layers of the canopy (cumulative LAI below 3). Field studies ; (E) N® (Woledge, 1988), (D) N­ (Woledge, 1988), (_) N® (Woledge
et al., 1992). Controlled environment study, (+) N®, (*) N­. The equation of the regression plotted in (C) is : % clover PAR capture ¯
(1±02³0±03) % clover LAI ­(4±4³2±6) ; n ¯ 46 ; r ¯ 0±96 ; P ! 0±001. The dashed lines show the confidence interval of the regression at P " 0±95.
$
capture by a planophile species like white clover. However,
the daily average of PAR interception in a natural
environment is better estimated by assuming 100 % diffuse
radiation (Varlet-Grancher and Bonhomme, 1979 ; Sinoquet
et al., 1990 ; Sinoquet and Bonhomme, 1992). With full
diffuse light, simulations show that the advantage of clover
was smaller in terms of PAR capture in the controlled
environment experiment (compare Figs 5 B and 8 A).
Nitrogen supply reduced, or even suppressed, the advantage of clover in terms of PAR capture (Fig. 8 A) : in the
field mixtures supplied with N fertilizer (reported by
Woledge, 1988) or the N­ treatment in the controlled
environment experiment, clover had no significant advantage, while the advantage was highly significant (P !
0±001 ; Wilcoxon’s sign test) for the low N treatments.
The reasons for clover’s advantage in terms of PAR
partitioning were further investigated by comparing different
radiative transfer simulations. First, we assumed for each
horizontal layer of the mixed canopy that grass and clover
had the same mean leaf angle, which was calculated as the
mean of the two species leaf angles. Simulations made
under this assumption, with the same data sets, show a clear
reduction in the advantage of clover PAR capture (compare
Fig. 8 A and B). Thus, even with fully diffuse radiation, the
planophile foliage of white clover partly explained its higher
PAR capture per unit leaf area.
By suppressing leaf angle effects, simulation allowed us to
test the effects of species vertical dominance. The vertical
dominance of clover was highly significant for the low N
treatments (P ! 0±001 ; Wilcoxon’s sign-test), but not for the
high N treatments (N­ in the controlled environment
experiment and supplied with N fertilizer in the study by
Woledge, 1988), which even displayed a tendency (P ! 0±06 ;
Wilcoxon’s sign test) towards vertical dominance of grass
(Fig. 8 B). This underlines that the vertical dominance of the
legume does hold in mixed swards with little or no inorganic
N supply, but not necessarily in mixtures grown with higher
nitrogen fertility.
44
Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards
Below a cumulative LAI of 3, simulations show that less
than 10 to 20 % of the incoming PAR is transmitted (Fig. 4).
Therefore, the contribution of clover to PAR capture by the
mixture is strongly related to its share of the total leaf area
in these upper (LAI ) canopy layers. The correlation between
$
both parameters was highly significant (Fig. 8 C) and close
to the 1 : 1 line :
% clover PAR capture ¯ (1±02³0±03) % clover
LAI ­(4±4³2±6)
$
Grass}clover differences in daily light interception are
thus accounted for mostly by the proportion of clover leaf
area in the upper (cumulative LAI below 3) canopy layers,
in good agreement with previous conclusions by Woledge
(1988) and Woledge et al. (1992). This means that the
interception efficiency of either component is strongly
determined by its ability to place its foliage at the top of the
mixed canopy.
Radiation use efficiency and growth
Leaves that are photosynthetically light saturated are less
efficient than those in the shade. Therefore, in a monoculture,
as the fraction of shade leaf area increases, RUE also
increases slightly (Sinclair and Horie, 1989). By contrast to
the monoculture, the fraction of leaf in the shade can reach
one for a shaded species grown in mixture. In this case, due
to the avoidance of light saturated photosynthesis, the
radiation use efficiency tends to increase (Willey, 1990). This
would explain the negative correlation between radiation
use efficiency and PAR capture per unit leaf area observed
for mixed grass and clover in our study (Fig. 6). According
to this hypothesis, the lower radiation use efficiency of the
legume would be due to its higher PAR capture per unit leaf
area. Interestingly, this would lead to a compensation
between the efficiencies of PAR capture by the components
and PAR use in a mixture. Such trade-offs can be illustrated
by the nitrogen supply effects in the controlled environment
experiment. At N­, the advantage of clover in PAR
capture per unit leaf area decreased by 28 % (from 153 to
110 µmol m−# s−") but RUE increased by 20 % (from 0±98 to
1±2 g DM mol−" PAR). Therefore, under conditions of high
N supply, mixed clover used radiation more efficiently.
However, several other factors could influence the
radiation use efficiency of mixed species in a natural
environment. First, crop radiation use efficiency has been
shown to increase with increased diffuse radiation (Sinclair,
Shiraiwa and Hammer, 1992). Moreover, as grass}clover
differences in PAR capture per unit leaf area were smaller
under full diffuse radiation (Fig. 8 A), the corresponding
differences in RUE could also be smaller in a natural
environment than those observed in a growth cabinet.
Second, an ANOVA on the residuals of the regression
indicates a significant effect (P ! 0±05) of species factor.
Therefore, the lower RUE of the legume should also be
ascribed to other components of the plant carbon balance,
like root and shoot respiration rates, which are larger with
white clover than with perennial ryegrass (Faurie, 1994).
Third, a decline in leaf N concentration at low N supply
could affect the grass RUE, by limiting the light saturated
rates of photosynthesis (Field and Mooney, 1986 ; Sinclair
and Horie, 1989 ; Be! langer, Gastal and Lemaire, 1992).
Nevertheless, in sharp contrast with results obtained with
grass monocultures (Be! langer et al., 1992), the mean grass
radiation use efficiency was 25 % higher at N® than at N­
(2±0 and 1±6 g DM mol−" PAR, respectively) in the controlled
environment mixtures. This discrepancy may originate from
the increased shading of grass leaves by clover at the low N
supply, resulting in a 27 % decline in the mean PAR capture
per unit leaf area of the grass in the upper canopy layer
(from 119 to 88 µmol PAR m−# s−").
Such trade-offs between PAR capture and PAR use could
help stabilize the botanical composition of mixed stands
during competitive growth periods. In good agreement with
a previous report by Davidson and Robson (1986), the
clover contents which were established at the time of canopy
closure did not vary significantly during the competitive
growth phase in the controlled environment experiment
(Table 1). Thus, under controlled environment conditions,
competition for light had only minor effects on the balance
between grass and clover.
This rather unexpected result can be better understood by
considering how light quality and quantity affect extension
of clover petioles (Solangaarachchi and Harper, 1987 ;
Thompson and Harper, 1988 ; Varlet-Grancher, Moulia and
Jacques, 1989). Clover avoids shade and reacts quickly to
shading by increasing its petiole length. Therefore, the ratio
of the extended length of clover petioles and grass leaves is
approximately constant (Davies and Evans, 1990). The
large plasticity of the legume tends, therefore, to buffer
competition for light in most situations. This plasticity has
hidden costs, however, like branching suppression (Simon,
Gastal and Lemaire, 1989) and the mortality of small shoot
growing points in dense canopies (Soussana, Verte' s and
Arregui, 1995).
Schwank et al. (1986) concluded that the growth potential
of clover in natural grasslands was determined by the PAR
intercepted by fully developed leaves in partly sunlit
positions. The present study supports this conclusion, but
also stresses that the balance between clover and grass
depends upon trade-offs between PAR capture and PAR
use and upon the morphogenetic costs of increased leaf size.
A C K N O W L E D G E M E N TS
We thank P. Pichon for expert technical assistance.
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