Annals of Botany 93: 699±710, 2004
doi:10.1093/aob/mch099, available online at www.aob.oupjournals.org
Effect of 3D Nitrogen, Dry Mass per Area and Local Irradiance on Canopy
Photosynthesis Within Leaves of Contrasted Heterogeneous Maize Crops
J . - L . D R O U E T 1 , * and R . B O N H O M M E 2
1Unite
 Mixte de Recherche INRA-INAPG Environnement et Grandes Cultures, BP 01, 78850 Thiverval-Grignon,
France and 2INRA Unite AgropeÂdoclimatique de la zone caraõÈbe, Domaine Duclos, 97170 Petit-Bourg, Guadeloupe,
France
Received: 24 October 2003 Returned for revision: 17 November 2003 Accepted: 13 February 2004 Published electronically: 8 April 2004
d Background and Aims Nitrogen partitioning within stands has been described fairly comprehensively, especially
for C3 plants in dense stands where the horizontal heterogeneity of foliage distribution is relatively small.
Nitrogen has been shown to be distributed vertically and in parallel to light, maximizing carbon assimilation and
stand productivity. Conversely, row crops such as maize (C4 plants) are characterized by strong horizontal heterogeneity of foliage distribution, and a three-dimensional (3D) approach is required to investigate the combined
effect of spatial distribution of nitrogen and light on canopy photosynthesis.
d Model The 3D geometry of maize canopies was modelled with varying densities and at different developmental
stages using plant digitizing under ®eld conditions. For lamina parts, photosynthesis was measured and nitrogen
content per unit area (Na) was described from analysis of nitrogen content per unit mass (Nm) and dry mass per
unit area (Ma). Hyperbolic relationships between photosynthesis at irradiance saturation (Pmax) and Na were
established as well as a linear relationship between dark respiration (Rd) and Na, whereas quantum ef®ciency (a)
was found to be independent of Na.
d Key Results and Conclusions N , M and N were shown to change over time vertically (i.e. between laminae),
m
a
a
which has been largely reported previously, and horizontally (i.e. within laminae), which has scarcely been
described previously. Even if Ma played a major role in Na, a strong relationship between Na and Ma could not
be demonstrated, whereas several previous studies have found that Na was essentially related to Ma rather than
Nm. From simulations of radiative exchange using a 3D volume-based approach and lamina photosynthesis using
a hyperbola, it was shown that real patterns of Na partitioning could increase daily crop photosynthesis by up to
8 % compared with uniform patterns of Na, especially for the earliest stages of stand development.
ã 2004 Annals of Botany Company
Key words: 3D plant architecture, heterogeneous crop, dry mass per unit area, irradiance, lamina, nitrogen content per
unit area, nitrogen content per unit mass, maize, photosynthesis, virtual plant, Zea mays.
INTRODUCTION
Nitrogen supply affects plant growth and productivity by
altering both leaf area and photosynthetic capacity (Novoa
and Loomis, 1981). About 75 % of leaf nitrogen is involved
in the photosynthetic processes (Evans, 1989) and its
partitioning inside canopies has been largely described
(see Grindlay, 1997, for review). Several authors have
observed vertical gradients of leaf nitrogen in crops
(Shiraiwa and Sinclair, 1993; Connor et al., 1995; Dreccer
et al., 2000), herbaceous plants (Field, 1983; Hirose and
Werger, 1987, Lemaire et al., 1991) and trees (DeJong and
Doyle, 1985; Hollinger, 1996). Leaf nitrogen is distributed
in parallel to light distribution (Anten et al., 1995; Kull and
Jarvis, 1995), which corresponds to the optimal distribution
of leaf nitrogen that maximizes carbon assimilation and
crop productivity (Mooney and Gulmon, 1979; Field, 1983;
Gutschick and Wiegel, 1988; Dreccer et al., 2000). Chen
et al. (1993) proposed an alternative theory called
coordination where canopy nitrogen is distributed so that
a balance is maintained between two processes depending
on nitrogen content: the Rubisco-limited rate of carboxyla* For correspondence. E-mail [email protected]
tion and the electron transport rate of carboxylation. They
found that carbon assimilation gain was similar, using either
the theory of coordination or optimization (Hirose and
Werger, 1987). These vertical gradients of nitrogen were
essentially observed within dense stands and the combined
effect of light and nitrogen on canopy photosynthesis was
assessed by using a vertical description of these two
variables (i.e. by canopy layer, a 1D approach). However,
studies within heterogeneous canopies have been scarce,
especially in row crops such as maize, sorghum, wheat and
sun¯ower (see Grindlay, 1997), and have seldom dealt with
the relationships between nitrogen and light gradients by
using a 3D approach (e.g. in maize, Drouet and Bonhomme,
1999). The effect of canopy heterogeneity on light interception has been assessed previously (Drouet et al., 1999),
but the combined effect of spatial distribution of nitrogen
and light on canopy photosynthesis within row crops has not
been investigated. Since light interception is an area-based
phenomenon (Biscoe and Gallagher, 1978), leaf photosynthesis has more often than not been simulated from leaf
nitrogen expressed per unit leaf area, Na (Field and Mooney,
1986; Sinclair and Horie, 1989). Na is the product of leaf
nitrogen per unit mass, Nm, and dry mass per unit area, Ma,
Annals of Botany 93/6, ã Annals of Botany Company 2004; all rights reserved
700
Drouet and Bonhomme Ð 3D Nitrogen, Dry Mass Per Area, Irradiance and Photosynthesis
and numerous studies have dealt with relationships between
Na and Ma, and between Na and Nm. Many authors have
shown that changes in Na were related to changes in Ma (i.e.
anatomical changes, Gulmon and Chu, 1981; DeJong et al.,
1989; Hirose et al., 1989; Ellsworth and Reich, 1993; Rosati
et al., 2000; Le Roux et al., 2001; Meir et al., 2002),
whereas various results have been found with changes in Na
related to Nm (i.e. chemical changes, Kull and Niinemets,
1993; Grassi et al., 2002). Moreover, results concerning
nitrogen partitioning related to irradiance and concerning
relationships between Na, Nm and Ma have been described
predominantly on C3 plants and rarely on C4 plants such as
maize. Those two groups of plants differ with regard to leaf
nitrogen content and photosynthesis: leaf nitrogen content is
lower for C4 plants than for C3 (Lemaire and Gastal, 1997)
and nitrogen use ef®ciency is higher for C4 plants than for
C3 (Gosse et al., 1986; Sage and Pearcy, 1987; Sinclair and
Muchow, 1999).
In an earlier paper (Drouet and Bonhomme, 1999), it was
shown that local leaf irradiance plays a major role in leaf
nitrogen partitioning within maize crops. In the present
study, two questions are addressed: (1) do nitrogen gradients
within and between laminae in relation to local irradiance
increase canopy photosynthesis compared with uniform
nitrogen partitioning, and (2) what is the source of the
variations in nitrogen per unit area, Na: changes in nitrogen
concentration, Nm, or in dry mass per unit area, Ma, or both?
MATERIALS AND METHODS
Experimental design
Two ®eld experiments were carried out in Grignon (France,
48°N, 2°E) using the maize (Zea mays L.) hybrid `DeÂa'. For
the ®rst one, maize was sown in the early summer of 1996 at
two initial densities: 20 plants m±2 (D-density) and 10 plants
m±2 (d-density). Each trial area comprised 40 rows, 50 m
long. Two `open-thinned' plots at low density were obtained
by removing plants during stem elongation from the area of
initial density 10 plants m±2, as follows. (1) Three plants out
of four were removed from within each row, which resulted
in a ®nal density of 2´5 plants m±2 (d10®2´5-density), and
(2) one row out of two was removed as well as nine plants
out of ten within the remaining row, which resulted in a ®nal
density of 0´5 plants m±2 (d10®0´5-density). For the second
experiment, maize was sown in the early summer of 1999 at
two initial densities: 30 plants m±2 and 10 plants m±2. One
plot at low density was obtained by removing plants during
stem elongation from one plot of initial density 10 plants
m±2. Three plants out of four were removed within each row,
which resulted in a ®nal density of 2´5 plants m±2. In both
experiments, one amount of mineral nitrogen (5´5 g m±2)
was applied at sowing. The plots were weeded and plants
were kept free of water stress by liberal drip irrigation.
Description of plant structure, lamina nitrogen and lamina
photosynthesis
In the ®rst experiment, the 3D geometric structure of the
plants was measured with a magnetic digitizing device
(Polhemus, 1993; see Sinoquet and Rivet, 1997, and Drouet,
2003, for more details). For each plant, the coordinates
along the axis of the stem and the midrib of each lamina
were recorded. The number of points per axis varied from
ten to 30 according to the length and the curvature of the
organ. To examine densities of 10 and 20 plants m±2, data
were obtained from 20 plants (four rows with ®ve plants per
row) at three stages of development: beginning of stem
elongation (60 days after sowing, DAS), end of stem
elongation (74 DAS) and post-silking (90 DAS). In both low
density plots (2´5 and 0´5 plants m±2), data were measured at
post-silking on 12 plants (four rows with three plants per
row). For each plot, the corresponding leaf area index (LAI)
is shown in Table 1. Measurements were taken in the
morning to minimize possible effects of wind, water stress
and solar position.
In the ®rst experiment, total nitrogen analyses were
carried out on the six central plants of each plot (two rows
with three plants per row). To study nitrogen partitioning
between laminae, the even-numbered laminae from 6 to 14
were analysed. Nitrogen partitioning within laminae was
assessed from analysis of nitrogen content on laminae 6
(located at the bottom of the canopy), 10 (in the middle of
the canopy) and 14 (at the top of the canopy). The velum of
each lamina was separated from the midrib and then
subdivided into two or three parts of equal length, according
to the length of the lamina. Dry mass was determined after
oven drying at 70 °C for at least 2 d. After crushing, total
TA B L E 1. Dates of measurements and corresponding developmental stage, plant density, leaf area index (LAI), and total
shoot nitrogen content within the plots
Days after
sowing, DAS
Developmental stage
60
60
74
74
90
90
90
90
Beginning of stem elongation
Beginning of stem elongation
End of stem elongation
End of stem elongation
Post-silking
Post-silking
Post-silking (after removing plants at 74 DAS)
Post-silking (after removing plants at 74 DAS)
Density (plants m±2)
LAI
Total shoot
nitrogen content (g)
D (20)
d (10)
D (20)
d (10)
D (20)
d (10)
d10®2´5 (2´5)
d10®0´5 (0´5)
4´5
2´9
6´4
4´3
6´7
4´9
1´1
0´2
0´42
0´56
0´74
1´02
0´79
1´41
2´13
2´30
Drouet and Bonhomme Ð 3D Nitrogen, Dry Mass Per Area, Irradiance and Photosynthesis
nitrogen (mineral and organic) content per unit mass (Nm)
was determined with a carbon±nitrogen analyser (ANA
1500 CN; Thermoquest, Les Ulis, France) based on the
Dumas method (dry process method, Dumas, 1831).
In both experiments, carbon dioxide assimilation was
measured at the lamina level by using a LI-6400 portable
photosynthesis system (LI-COR, Inc., NB, USA). Photosynthesis±irradiance response curves were obtained by
measuring photosynthesis successively at 500, 200, 150,
100, 50, 500, 1000, 1500 and 2000 mmol PAR m±2 s±1.
Lamina photosynthesis at irradiance saturation was
measured at 2000 mmol PAR m±2 s±1 (P2000). Samples
were taken from the bottom (i.e. lamina 6) to the top (i.e.
lamina 14) of the canopy, at several dates around silking
within the plots at densities of 20 and 10 plants m±2 in 1996,
and within the plots at densities of 30, 10 and 2´5 plants m±2
in 1999 (Table 2). All measurements of lamina photosynthesis were carried out between 0800 and 1100 h (see
Bunce, 1990). Total nitrogen analyses were carried out on
all samples where photosynthesis was measured.
Reconstruction of 3D shoot structure and restitution of
lamina nitrogen
The reconstruction of the 3D shoot structure (Fig. 1A, B)
and the restitution of lamina nitrogen partitioning (Fig. 1C,
D) has been described in Drouet and Bonhomme (1999) and
Drouet (2003). Dry mass per unit lamina area (Ma) was
evaluated from dry mass and lamina area estimated
from allometric relationships between lamina length and
maximal width (Bonhomme and Varlet-Grancher, 1978).
Nitrogen content per unit area (Na) was determined from Nm
and Ma. Each plant was geometrically represented by a set
of about 1000 triangles and individual values of Nm, Ma and
Na were assigned to each triangle.
Simulation of light distribution and canopy photosynthesis
A 3D volume-based version of the light transfer model
RIRI (Radiation Interception in Row Intercropping,
Sinoquet and Bonhomme, 1992) was used to calculate
irradiance distribution inside the canopies. It had previously
been validated using radiation measurements for several
crops, especially maize canopies (see Sinoquet and
Bonhomme, 1989, 1992). This model is based on the
turbid-medium analogy. In this method, the canopy structure is abstracted by an array of 3D cells (0´1 m wide), which
may contain foliage or be empty. For each canopy cell, the
lamina area density, the lamina angle distribution (not
shown) and the lamina nitrogen content (Fig. 1C, D) are
calculated from the area, the orientation and the nitrogen
content of the triangles (Fig. 1A, B) (B. Andrieu, pers.
comm.). The model deals with direct and diffuse incident
radiation and scattered radiation, which makes it possible to
obtain, within each cell of the canopy, the instantaneous
lamina irradiance for sunlit and shaded lamina area (for
more details, see Sinoquet and Bonhomme, 1992; Drouet,
1998). For each plot, simulations were performed in
the photosynthetic active radiation waveband (PAR,
400±700 nm) from six values of daily global radiation
701
TA B L E 2. Dates and types of measurements for lamina
photosynthesis: photosynthesis at 2000 mmol PAR m±2 s±1
(P2000) and photosynthesis±irradiance curves [P(I)]
Days after
sowing, DAS
Year
Density
(plants m±2)
Type of
measurements
66
67
79
81
83
85
87
87
95
96
97
97
97
1999
1999
1999
1999
1996
1996
1999
1999
1999
1996
1996
1999
1999
10
30
30
30
20
20
30
2´5
2´5
20
20
10
30
P(I)
P(I)
P(I)
P(I)
P(I)
P2000
P2000
P2000
P(I)
P(I)
P2000
P(I)
P(I)
Dates of silking were 87 DAS in 1996 and 90 DAS in 1999.
(Table 3). Instantaneous values of direct radiation and
diffuse radiation were simulated for each time step (0´1 h)
according to Spitters et al. (1986) and J.-M. Allirand ( pers.
comm.). For each cell of the canopy, the daily average
lamina irradiance (Id,a) was computed from the instantaneous values (Fig. 1E, F). The model relies upon the optical
properties of the foliage. We found that re¯ectance and
transmittance were independent of Na, at least during the
period studied (data not shown). Consequently, only one
average value of re¯ectance/transmittance was used (0´07).
Soil re¯ectance was set equal to 0´10 (for more details, see
Drouet, 1998).
Lamina photosynthesis in response to irradiance was
simulated by using a rectangular hyperbola (Chartier, 1966,
1969; Thornley, 1976):
Pn,i,a(I) = (Pmax aI)/(Pmax + aI) ± Rd
(1)
where Pn,i,a is net instantaneous photosynthesis per unit
lamina area, I is PAR, Pmax is photosynthesis at irradiance
saturation, a is quantum ef®ciency and Rd is dark respiration.
Pachepsky et al. (1996) indicated that such a model is
quite adequate to predict quantitatively the biomass production of crops and has the advantage of requiring few
parameters. These authors pointed out that it is not
necessary to introduce into crop models more complicated
and more sophisticated descriptions of photosynthesis.
Pmax, a and Rd were ®tted by non-linear regression between
Pn,i,a and I.
Pmax as a function of Na was modelled by using a
hyperbola (Sinclair and Horie, 1989). As photosynthesis
was measured at 2000 mmol PAR m±2 s±1, this model was
used to simulate P2000 as a function of Na:
P2000(Na) = P2000,max [2/{1 + exp[±b (Na ± N0)]} ± 1]
(2)
where P2000,max, b and N0 are three parameters ®tted by nonlinear regression to the median P2000 value for each 0´2 g m±2
range in Na (Muchow and Sinclair, 1994).
702
Drouet and Bonhomme Ð 3D Nitrogen, Dry Mass Per Area, Irradiance and Photosynthesis
F I G . 1. Three-dimensional (3D) description of the aerial structure within a 10-plant m±2 canopy (d-density) at two developmental stages (60 and 90
DAS), with corresponding vertical pro®les (by canopy tube, 2D representation) of lamina nitrogen content per unit area (Na), daily average lamina
irradiance (Id,a) calculated for a sunny day (25 MJ m±2) and net daily photosynthesis per unit lamina area (Pn,d,a).
Pmax derives from P2000, and Dwyer and Stewart (1986)
pointed out that the variability in P2000 is lower than that in
Pmax.
a and Rd were assumed to vary linearly with Na (Hirose
and Werger, 1987, Muchow and Sinclair, 1994):
(3)
a(Na) = aa + ba Na
Drouet and Bonhomme Ð 3D Nitrogen, Dry Mass Per Area, Irradiance and Photosynthesis
Rd(Na) = aRd + bRd Na
(4)
where aa, ba, aRd and bRd are parameters.
For each cell of the canopy, the net daily photosynthesis
per unit lamina area (Pn,d,a, Fig. 1G, H) was computed by
summing the instantaneous values (Pn,i,a). The net daily
photosynthesis of the whole canopy (Pn,d,c) resulted from
the sum of Pn,d,a (de Wit, 1965).
TA B L E 3. Characteristics of the daily incident radiation
simulated for the six values of daily global radiation used in
computations of light absorption
Daily global radiation
(MJ m±2)
5
10
15
20
25
30
Daily ratio diffuse radiation/global
radiation
1´00
0´89
0´79
0´61
0´43
0´25
703
To quantify the photosynthetic bene®t of real Na partitioning, we compared Pn,d,c values between real and
associated hypothetical canopies. For each studied canopy,
two hypothetical canopies were generated by redistributing
Na from the real partitioning. In the ®rst one, Na was
redistributed uniformly along the velum by using, for each
lamina, its mean Na value. In the second one, Na was
redistributed uniformly within the whole canopy corresponding to the mean value of Na within the canopy.
Data were analysed (regression tests, mean comparisons,
graphs) using the S-PLUS computer package (S-PLUS,
1996).
RESULTS
Photosynthetic capacity of laminae
The relationship between P2000 and Na was described by
using the hyperbolic model proposed by Sinclair and Horie
(1989) (Fig. 2A, B). Before silking, ®tted values of the
parameters b and N0 (Table 4) were close to those found by
Muchow and Sinclair (1994): 2´45 vs. 3´68 for b and 0´27 vs.
0´20 for N0. Conversely, values of P2000,max strongly varied
F I G . 2. Relationships between net instantaneous photosynthesis per unit lamina area (Pn,i,a) and lamina nitrogen content per unit area (Na).
(A, B) Relationships between net photosynthesis at 2000 mmol PAR m±2 s±1 and Na (see Sinclair and Horie, 1989, P2000(Na) = P2000,max [2/{1 +
exp[±b (Na ± N0)] ± 1}]. (A) Before silking, and (B) after silking. (C) Quantum ef®ciency and Na [a(Na) = aa + ba Na]. (D) Dark respiration and
Na [Rd(Na) = aRd + bRd Na].
704
Drouet and Bonhomme Ð 3D Nitrogen, Dry Mass Per Area, Irradiance and Photosynthesis
TA B L E 4. Parameters of the relationship between net photosynthesis per unit lamina area (Pn,i,a) and nitrogen content per
unit area (Na)
Parameters
Variable
(1)
Number of
samples
P2000,max
(mmol CO2 m±2 s±1)
b (m2 g±1)
N0 (g m±2)
RSE (mmol
CO2 m±2 s±1)
R2
P2000(Na)
(before silking)
P2000(Na)
(after silking)
(2)
39
36´8 6 4´2
2´45 6 0´92
0´27 6 0´14
3´8
0´64 (P < 0´001)
18
40´2 6 5´1
1´41 6 0´78
0´43 6 0´26
2´6
0´78 (P < 0´001)
a(Na)
(3)
18
ba (mmol PAR
mmol±1 CO2 g±1 m2)
± 0´001
bRd (mmol CO2 g±1 s±1)
Rd(Na)
18
aa (mmol PAR
mmol±1 CO2)
0´044
aRd (mmol
CO2 m±2 s±1)
±2´14
2´30
RSE (mmol PAR
mmol±1 CO2)
0´009
RSE (mmol
CO2 m±2 s±1)
0´67
0´003 (P = 0´84)
0´64 (P < 0´001)
Parameters of the relationships between (1) net photosynthesis at 2000 mmol PAR m±2 s±1 and Na (see Sinclair and Horie, 1989; Muchow and
Sinclair, 1994; P2000(Na) = P2000,max [2/{1 + exp[±b(Na ± N0)]} ± 1] before silking (see Fig. 2A) and after silking (see Fig. 2B), (2) quantum ef®ciency
and Na; a(Na) = aa + ba Na (see Fig. 2C), (3) dark respiration and Na; Rd(Na) = aRd + bRd Na (see Fig. 2D).
between our ®tted values and those found by these authors
(36´8 vs. 52´0). This difference can be explained by different
climatic conditions, and consequently different photosynthetic capacity of laminae, between the two experimental
sites, especially the air temperature: 21±22 °C in Grignon
(48°N) vs. 28±30 °C in Australia (14°S). After silking, the
values of the parameters b and N0, and consequently the
shape of the P2000(Na) curve, changed: 1´41 after silking vs.
2´45 before silking for b and 0´43 vs. 0´27 for N0, while
P2000,max changed slightly (40´2 vs. 36´8).
A similar behaviour was found between the pre- and postsilking photosynthetic measurements for quantum ef®ciency, a (Fig. 2C), on the one hand and for dark respiration
Rd (Fig. 2D) on the other. No effect of Na was found on a,
while Rd varied linearly with Na (Table 4). These results are
in accordance with the literature (e.g. Schieving et al., 1992;
Connor et al., 1993; Anten et al., 1995), except for ®ndings
by Hirose and Werger (1987) and Muchow and Sinclair
(1994), who proposed a linear relationship between a and
Na, and for ®ndings by Pons et al. (1989) who proposed a
curvilinear relationship between a and Na.
The model of lamina photosynthesis was globally
assessed by comparing the simulated values of Pn,i,a
(Pn,i,a,sim) from P2000(Na), a and Rd(Na) with the observed
values (Pn,i,a,obs). We obtained Pn,i,a,sim = 1´001 6 0´01
Pn,i,a,obs ± 0´251 6 0´211 (P value = 0´0001, R2 = 0´97).
Thus, the model with its parameterization is a suitable
description of lamina photosynthesis.
Nm, Ma and Na partitioning within and between laminae
Results for Na have been described in a previous paper
(Drouet and Bonhomme, 1999). The main trends for Na are
recalled here in order to point out the links between Na, Nm
and Ma.
Partitioning along the velum (Table 5). At the beginning
of stem elongation (60 DAS) under both density conditions
(D- and d-density), Nm and Ma increased from the base to
the tip of velums 6 and 10, especially between the base and
the middle of the velum for Nm (signi®cant at P < 0.05) and
between the middle and the tip of the velum for Ma (P <
0.05). This produced a signi®cant increase in Na from the
base to the tip of velums 6 and 10. At the end of stem
elongation (74 DAS), the same behaviour was observed for
laminae 10 and 14 in both densities: Nm and Ma increased
from the base to the tip of the velum (only between the
middle and the tip of the velum for Ma), producing an
increase in Na. At post-silking (90 DAS), slight variations in
Nm and Ma in the opposite direction generated slight
variations in Na along velum 6. This behaviour was also
observed for velum 10, but only in the D-density. For velum
10 in d-, d10®2´5- and d10®0´5-densities, Nm and Ma also
varied slightly in the opposite direction and no signi®cant
change was observed for Na. Nm remained constant along
velum 14 in all densities, while Ma decreased signi®cantly.
A signi®cant decrease in Na was also observed from the base
to the tip of velum 14, except in the D-density.
Partitioning between laminae (Fig. 3). Regarding
changes in Nm, Ma and Na between laminae over time (Ddensity, Fig. 3, ®rst line), signi®cant differences were
observed (P < 0.05) in Nm between laminae and between
dates of measurements. Nm varied slightly around the mean
values. Whatever the date, no strong gradient in Nm was
observed between laminae. On the contrary, Ma in lower
laminae, which had ®nished their growth (i.e. laminae 6 and
8), varied very slightly with no signi®cant difference
between mean values. Growing laminae had lower values
of Ma than mature ones (e.g. for lamina 12, mean values of
Ma increased from 33´2 g m±2 at 60 DAS to 56´6 g m±2 at
90 DAS). Strong gradients in Ma were observed between
laminae (e.g. at 90 DAS, mean values of Ma varied from
40´7 g m±2 for lamina 6 to 56´6 g m±2 for lamina 12).
Consequently, Na varied slightly over time in the laminae
that had ®nished their growth (i.e. laminae 6 and 8) and
Drouet and Bonhomme Ð 3D Nitrogen, Dry Mass Per Area, Irradiance and Photosynthesis
705
F I G . 3. Lamina nitrogen content per unit dry mass (Nm), dry mass per unit area (Ma) and nitrogen content per unit area (Na) as a function of lamina
rank within (A±C) a 20-plant m±2 canopy (D-density) at three developmental stages (60, 74 and 90 DAS) and (D±F) within canopies of various
densities (D-, d-, d10®2´5- and d10®0´5-density) at post-silking (90 DAS). Each point represents six plants.
increased in growing laminae (i.e. laminae 10, 12 and 14
between 60±90 DAS). At post-silking (90 DAS), a gradient
in Na was observed from the bottom to the top of the canopy.
This may be the result of nitrogen remobilization from the
lower laminae to the upper ones, nitrogen absorption and
growth in Ma (and lamina thickness) of developing laminae.
Regarding changes in Nm, Ma and Na between laminae as a
function of plant density at post-silking (Fig. 3, second line),
Nm increased signi®cantly (P < 0.05) from the bottom to the
top of the dense canopies (D- and d-density). Variations in
Nm were not apparent in the open-thinned canopies (d10®2´5and d10®0´5-density). Consequently, an increase in Nm from
dense to open canopies was observed for lower laminae (i.e.
laminae 6 and 8), while Nm remained relatively constant
between dense and open canopies for upper laminae (i.e.
laminae 10±14). Similar vertical pro®les of Ma were
observed between densities, with higher values of Ma in
the open canopies (d10®2´5- and d10®0´5-density) than in the
dense ones (D- and d-density). Consequently, the pro®les of
Na partitioning were characterized by a stronger vertical
gradient in the dense canopies (D-density) than in the open
ones.
DISCUSSION
Contribution of a 3D approach to simulate canopy
photosynthesis within heterogeneous row crops
Changes in Na along the velum (i.e. `horizontal' changes)
were essentially observed until stem elongation (Table 5),
whereas changes in Na between laminae (i.e. `vertical'
changes) were observed after stem elongation (Fig. 3C). The
effect of Na partitioning within canopies was quanti®ed by
comparing the daily net photosynthesis (Pn,d,c) between real
and associated hypothetical canopies. Before stem elongation within the dense canopy (D-density), real Na partitioning (Table 5 and Fig. 3) made it possible to increase Pn,d,c
from 1 to 7 % compared with uniform Na along each velum,
and from 2 to 8 % compared with uniform Na within the
whole canopy (Fig. 4A). After stem elongation, which
corresponded to canopy closure, similar behaviour was
observed but the increase in Pn,d,c was lower: from 2 to 4 %
in the ®rst case and from 4 to 6 % in the second. After
silking, gradients along the velum were not signi®cantly
different in most canopies (Table 5) that involved no
difference in Pn,d,c between the real D-density canopy and
706
Drouet and Bonhomme Ð 3D Nitrogen, Dry Mass Per Area, Irradiance and Photosynthesis
TA B L E 5. Mean of nitrogen content per unit dry mass (Nm), dry mass per unit area (Ma) and nitrogen content per unit
area (Na) in each part of the velum (base, middle and tip) of laminae 6 (bottom of the canopy), 10 (middle of the canopy)
and 14 (top of the canopy) within the eight plots
Days after
sowing, DAS
Density
60
D
60
d
74
D
74
d
90
D
90
d
90
d10®2´5
90
d10®0´5
Velum Nm (g N kg±1 DM)
Velum Ma (g m±2)
Velum Na (g m±2)
Lamina
rank
Base
Middle
Tip
Base
Middle
Tip
Base
Middle
Tip
6
10
6
10
10
14
10
14
6
10
14
6
10
14
6
10
14
10
14
26´4b
19´9b
30´5b
20´7c
24´4b
22´0b
25´1c
23´1b
20´4b
23´2c
30´8a
28´3a
28´2b
33´4a
34´0a
30´7b
33´2a
27´1b
32´4a
32´1a
26´2a
36´9a
27´6b
32´2a
±
33´6b
±
±
29´0b
±
±
34´5a
±
±
36´2a
±
33´4a
±
32´7a
29´1a
38´5a
33´7a
34´3a
29´6a
38´0a
29´6a
22´7a
30´3a
31´1a
28´6a
32´9a
34´0a
34´1a
34´6a
35´3a
32´7a
33´5a
38´3b
27´5c
40´4b
27´5c
41´1b
34´5a
52´2ab
31´2a
39´3a
47´8ab
49´7a
42´0a
57´5a
51´6a
54´0a
66´7a
57´3a
72´3a
57´7a
36´7b
37´5b
39´2b
35´9b
44´5b
±
45´3b
±
±
43´3b
±
±
47´1b
±
±
53´0b
±
57´8b
±
45´3a
43´8a
45´5a
46´7a
53´3a
33´2a
56´3a
40´5a
36´3a
50´9a
44´1b
38´1b
53´7a
42´2b
48´6b
57´5b
45´1b
60´7b
44´2b
1´01b
0´55c
1´23c
0´57c
0´99c
0´76b
1´31b
0´72b
0´80a
1´11b
1´53a
1´19a
1´63a
1´72a
1´83a
2´05a
1´91a
1´96a
1´87a
1´18b
0´98b
1´45b
0´99b
1´43b
±
1´52b
±
±
1´25b
±
±
1´62a
±
±
1´92a
±
1´93a
±
1´48a
1´27a
1´75a
1´57a
1´83a
0´98a
2´14a
1´21a
0´82a
1´55a
1´37a
1´09a
1´77a
1´43b
1´66a
1´99a
1´59b
1´98a
1´48b
Each mean is estimated from six plants. For each line and for each variable (Nm, Ma, Na), means with the same letter (a, b, c) are not signi®cantly
different at P < 0.05 (Student±Newman±Keuls test)
F I G . 4. Mean and standard deviation of the normalized daily net photosynthesis (Pn,d,c) of real and associated hypothetical canopies for which either
Na partitioning is uniform along each lamina (changes in Na partitioning between laminae only, see Fig. 3) or Na partitioning is uniform within the
whole canopy. Comparisons between real and associated hypothetical nitrogen partitioning are shown for (A) a 20-plant m±2 canopy (D-density) at
three developmental stages (60, 74 and 90 DAS), and (B) within canopies of various densities (D-, d-, d10®2´5-density) at post-silking (90 DAS). For
each plot, the values of Pn,d,c simulated within the hypothetical canopies are normalized by the value of Pn,d,c simulated within the associated real
canopy. Mean and standard deviation are calculated with the six daily incident radiation characteristics shown in Table 3.
its associated hypothetical canopy with uniform Na along
the velum. On the contrary, strong gradients in Na between
laminae (Fig. 3C) involved increased Pn,d,c from 5 to 7 %
compared with uniform Na within the whole canopy
(Fig. 4A). This behaviour was also observed within the ddensity canopy, but the difference between real and
hypothetical canopies was lower: Pn,d,c increased by 2 %
after silking (Fig. 4B). For the open-thinned canopies, Na
gradients within and between laminae had disappeared, and
the real Na partitioning gave similar Pn,d,c to uniform Na
within laminae and within the whole canopy (Fig. 4B). The
®rst hypothesis for Na partitioning (vertical Na gradients
only) is thus valuable for the dense canopies after stem
elongation. The second one, which does not take into
Drouet and Bonhomme Ð 3D Nitrogen, Dry Mass Per Area, Irradiance and Photosynthesis
account Na partitioning to simulate photosynthesis and
biomass production, is valuable for the open-thinned
canopies where no horizontal and vertical gradients were
observed.
In heterogeneous canopies, vertical descriptions of Na
partitioning can be used in dense ones to simulate canopy
photosynthesis (e.g. Hirose and Werger, 1987; Anten at al.,
1995; Dreccer et al., 2000), even if a vertical exponential Na
partitioning underestimated Pn,d,c (Dreccer et al., 2000). But
when lamina area density partitioning varies greatly along
an axis perpendicular to the row direction (d-density,
Fig. 1A, B), simulations indicated differences of canopy
photosynthesis up to 8 % between real and associated
hypothetical canopies. That involved taking into account
spatial variations in Na (i.e. Na within and between laminae)
by using 3D representations of the canopy variables.
However, those differences are within the range of error
of photosynthesis measurements in canopies.
In the open-thinned canopies (d10®2´5- and d10®0´5density), total shoot nitrogen content increased within the
plant compared with the d-density canopy: from 1´41 g per
plant to 2´13 g per plant after the moderate thinning and
from 1´41 g per plant to 2´30 g per plant after the strong
thinning (Table 1). Thinning plants involved uniform Na
partitioning, with Na tending towards a maximal value
around 2 g m±2 (Fig. 3F, see Drouet and Bonhomme, 1999),
which might correspond to the maximal photosynthetic
capacity of laminae. Simulations indicated that Na partitioning after removing plants involved an increase in Pn,d,c
from 6 to 7 % within the open-thinned canopies compared
with the Na partitioning within the d-density canopy.
Because of foliage heterogeneity within the open-thinned
canopies, 3D representations of the canopy variables were
needed. But it was shown that, in our experimental openthinned canopies, this approach was not ®nally necessary
because of uniformity of Na and Id,a partitioning (see Drouet
and Bonhomme, 1999).
Spatial changes in Na partitioning: changes in Nm or
regulation by Ma?
Na is the product of Nm and Ma. Increased Ma is the result
of increased lamina thickness (Maurice et al., 1997) and
increased lamina density (Witkowski and Lamont, 1991).
Relationships between Na and Nm and between Na and Ma
for all canopies indicated that changes in Na jointly result
from changes in Nm and Ma (Fig. 5). However, the
relationship between Na and Ma was better (Table 6; RSE
= 0´21 and R2 = 0´78) than that between Na and Nm (RSE =
0´28 and R2 = 0´61).
For each canopy, the relationship between Na and Nm was
slightly stronger than that between Na and Ma at the
beginning of stem elongation. At this stage, we can consider
that Nm and Ma contributed equally to the variability of Na.
Nm and Ma decreased simultaneously from the bottom to the
top of the D-density (Fig. 3A, B) and d-density canopies
(data not shown), which produced a decrease in Na. At the
end of stem elongation, the tendency reversed: the relationship between Na and Nm was slightly weaker than that
between Na and Ma. The vertical partitioning of Nm
707
remained constant, whereas Na changed between laminae
in the same way as Ma, which corresponded to vertical
gradients of Id,a.
At post-silking, the relationship between Na and Ma was
better than that between Na and Nm, except in the D-density
canopy. Vertical Na distribution (Fig. 3C) corresponded
with vertical Id,a distribution (see Drouet and Bonhomme,
1999), except at the top of the canopy where low Na values
were observed within the most illuminated laminae
(Fig. 1F). That might be due to Na remobilization from
not only lower but also upper laminae towards the grains
already developed at this period. This hypothesis agrees
with results from several authors (e.g. Crafts-Brandner and
Poneleit, 1987; Thomas and Smart, 1993; Sadras et al.,
1993, 2000), who indicated an effect of reproductive growth
on lamina senescence and lamina nitrogen partitioning. The
latter in particular showed that the important changes in the
pro®le of lamina nitrogen in maize and sun¯ower during
grain ®lling were unrelated to the light regime. Vertical
gradients were also observed in Ma (Fig. 3B), whereas
vertical gradients in Nm were not apparent (Fig. 3A). In the
open-thinned canopies, no correlation was found between
Na and Nm (R2 = 0´09), whereas clear relationships were
observed between Na and Ma (Table 6). These observations
suggest that changes in Na might result from changes in Ma
rather than changes in Nm, but this result was not as obvious
as in previous studies (e.g. Hirose et al., 1989; Ellsworth and
Reich, 1993; Rosati et al., 2000; Le Roux et al., 2001). Ma
distribution therefore cannot provide a means of distributing
Na within plant canopies, contrasting with results from
Ellsworth and Reich (1993), for example, who found that
the distribution of Ma in tree canopies explained 95 % of the
distribution of Na in Acer saccharum. Furthermore, Hirose
et al. (1988) showed that Ma in the canopy was controlled
not only by light climate but also by nitrogen availability to
each lamina. Light distribution therefore cannot provide a
means of predicting Ma (and consequently Na) distribution,
even if light plays a major role in Ma and Na distribution.
CONCLUSIONS
By using one cultivar of maize grown during a single
season, it was shown that Na partitioning was closely related
to the heterogeneity of irradiance within maize canopies
until silking. Using a 3D approach to describe lamina
nitrogen and irradiance, it was shown that the real patterns
of Na partitioning could increase daily canopy photosynthesis by up to 8 % compared with uniform patterns of Na.
That was especially observed for the earliest stages of
development where lamina area density partitioning varies
greatly along an axis perpendicular to the row direction. In
row heterogeneous crops, the classical approach of vertical
gradients for nitrogen and light within dense canopies
therefore could not be applied and a 3D description of the
canopy variables (irradiance, Nm, Ma, Na) would be
required. Most studies have shown that Na is related to
dry mass per unit area (Ma) rather than nitrogen concentration (Nm). Our data indicated that, even if Ma plays a major
role in Na, we cannot evidence a strong relationship between
708
Drouet and Bonhomme Ð 3D Nitrogen, Dry Mass Per Area, Irradiance and Photosynthesis
F I G . 5. Lamina nitrogen content per unit area (Na) as a function of (A) nitrogen content per unit dry mass (Nm), and (B) dry mass per unit area (Ma)
for four densities at three developmental stages (D- and d-density at 60, 74 and 90 DAS, d10®2´5- and d10®0´5-density at 90 DAS).
TA B L E 6. Parameters of the linear adjustment (a) between lamina nitrogen content per unit area (Na) and lamina nitrogen
content per unit dry mass (Nm): Na = aNaNm + bNaNmNm, and (b) between lamina nitrogen content per unit area (Na) and
lamina dry mass per unit area (Ma): Na = aNaMa + bNaMaMa. RSE, residual standard error
Days after
sowing, DAS
(a) Na and Nm
60
60
74
74
90
90
90
90
All canopies
(b) Na and Ma
60
60
74
74
90
90
90
90
All canopies
Density
(plants m±2)
Number of
samples
D
d
D
d
D
d
36
36
30
30
42
42
42
30
288
±0´41
±0´62
±0´71
±0´93
±0´49
±0´46
0´86
2´57
±0´62
6
6
6
6
6
6
6
6
6
0´12
0´12
0´24
0´28
0´14
0´34
0´49
0´44
0´10
D
d
D
d
D
d
36
36
30
30
42
42
42
30
288
±0´58
±0´85
±0´61
±0´47
±0´68
±0´17
0´36
0´80
±0´34
6
6
6
6
6
6
6
6
6
0´19
0´17
0´17
0´19
0´19
0´16
0´18
0´14
0´06
d10®2´5
d10®0´5
d10®2´5
d10®0´5
Na and Ma. Na partitioning resulted mostly from Ma
partitioning but also from Nm partitioning.
ACKNOWLEDGEMENTS
The authors are grateful to Dr V. O. Sadras and Dr N. P. R.
Anten for valuable suggestions when reviewing the manuscript. We acknowledge Dr H. Sinoquet for valuable
consultations concerning his RIRI model and, with P.
Rivet, on the digitizing system, Polhemus. We thank Dr B.
Andrieu for providing us with his `surface-to-volume'
Intercept a
(g m±2)
Slope b
(kg DM m±2)
RSE
(g m±2)
kg DM m±2 for Na vs. Nm relationship
0´054 6 0´004
0´14
0´060 6 0´004
0´14
0´067 6 0´008
0´22
0´077 6 0´009
0´29
0´063 6 0´005
0´14
0´062 6 0´011
0´23
0´029 6 0´014
0´24
±0´023 6 0´014
0´20
0´067 6 0´003
0´28
Dimensionless for Na vs. Ma relationship
0´043 6 0´005
0´18
0´054 6 0´004
0´18
0´044 6 0´004
0´18
0´041 6 0´004
0´25
0´042 6 0´004
0´17
0´035 6 0´003
0´16
0´027 6 0´003
0´15
0´018 6 0´002
0´12
0´038 6 0´001
0´21
R2
0´82
0´88
0´70
0´72
0´79
0´45
0´09
0´09
0´61
0´71
0´83
0´81
0´79
0´71
0´74
0´65
0´68
0´78
procedure. Thanks to F. Lafouge for the nitrogen analysis,
as well as P. BonchreÂtien, M. Lauransot, C. Civet, A.
Fortineau and M. and J. Chartier for their technical
assistance. S. Tanis-Plant gave us editorial advice.
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