Directory UMM :Data Elmu:jurnal:E:European Journal of Agronomy:Vol13.Issue2-3 July2000:
Effect of crop nitrogen status and temperature on the
radiation use efficiency of winter oilseed rape
Eric Justes
a,*, Pascal Denoroy
b,1, Benoit Gabrielle
b, Ghislain Gosse
baINRA,Unite´ d’Agronomie de Chaˆlons-Reims,2Esplanade Roland Garros,BP 224,F-51686 Reims cedex 2, France bINRA,Unite´ de Bioclimatologie,F-78850Thi6er6al-Grignon, France
Received 19 February 1999; received in revised form 7 July 1999; accepted 18 January 2000
Abstract
In temperate environments, the total dry matter (TDM) of a crop is closely related to the amount of photosynthet-ically active radiation absorbed (SPARa), as long as other factors (water, nutrients, . . .) are non-limiting. For oilseed rape crops, many authors have shown that the radiation use efficiency (RUEa) varies within a wide range, from 1 to 4 g MJ−1 of SPARa according to developmental stage and environmental conditions. In order to explain this
variability, effects of N and temperature on RUEa were investigated during a 1-year field experiment involving three N treatments (N fertilisation rates: 0, 135 and 270 kg ha−1). Leaf, flower, and pod surface areas, as well as the DM
and N content of the various plant parts were measured every 2 – 4 weeks for 17 sampling dates from emergence to harvest. RUEa was calculated from total generated DM (shoot and root DM, plus that of dead leaves fallen to the ground). Daily PARa was calculated using a 3-layer model taking into account leaf and pod absorption and reflection of PAR by flowers and soil. The N nutrition index (NNI) proposed by Lemaire and Gastal (1997) was used to evaluate the N effect on RUEa. NNI was significantly higher than the critical N value (meaning that N was non-limiting) for the N270 treatment from emergence to pod formation, but N deficiency occurred with N0 at the 12-leaf stage and later with N135 at flowering. The maximum possible RUEa (RUEamax) was assumed to be the value
obtained with the treatment N270, where N was non-limiting. The N deficiencies which occurred for N0 and N135 significantly reduced the green LAI and PAI, and consequentlySPARa. To remove any effect other than N on the RUEa, the ratio of actual to maximum RUEa (RUEa/RUEamax) proposed by Be´langer et al. (1992) was calculated
for each developmental stage of oilseed rape. A linear regression fit well (R2=0.919; 8 d.f.) the response of
RUEa/RUEamaxversus N deficiency, for values of NNI lower than 1. The resulting equation was the following:
RUEa/RUEamax=0.74×NNI+0.23. RUEamaxwas also significantly affected by developmental stage. Whereas the
corresponding changes in RUEamaxfrom the 6-leaf stage to the end of flowering could be related to air temperature,
there was evidence of a developmental effect in the other stages. RUEa was lower in the early stages (emergence to 5 – 6 leaves), and from pod formation until ripening; the latter decrease could be attributed to the high energy cost of lipid biosynthesis. © 2000 Elsevier Science B.V. All rights reserved.
Keywords:Oilseed rape; Radiation use efficiency; Nitrogen; Temperature; Development stage
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* Corresponding author. Tel.: +33-3-26773588; fax: +33-3-26773591. E-mail address:[email protected] (E. Justes).
1Present address: INRA, Unite´ d’Agronomie, BP 81, F-33833 Villeneuve d’Ornon cedex, France.
1161-0301/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved. PII: S 1 1 6 1 - 0 3 0 1 ( 0 0 ) 0 0 0 7 2 - 1
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1. Introduction
The efficiency of conversion of solar energy into biomass by a crop is usually represented by a synthetic value which is the conversion effi-ciency of intercepted radiation or radiation use efficiency (RUE) (Monteith, 1972). The RUE is defined as the quantity of dry biomass (DM) produced per unit of radiation intercepted or absorbed by the crop. The radiation used may be either: (i) the total short wave radiation (R; Ri for intercepted R, Ra for absorbed R); or (ii) the photosynthetically active radiation (PAR; PARi for intercepted PAR, PARa for absorbed PAR) (Varlet-Grancher et al., 1989). The value of the RUE is expressed in grams of aerial dry matter (ADM) or total dry matter (TDM) (shoots+
roots) per megajoule of radiation (g MJ−1); it
varies depending on whether it is calculated as PAR absorbed (RUEa) or as PAR intercepted (RUEi).
The RUE of oilseed rape has already been estimated by several authors, whose values show a great deal of variability. For example, accord-ing to Mendham et al. (1981), the RUEi calcu-lated on the basis of the aerial parts of oilseed rape until flowering, without any stress, was on average 2.4 g MJ−1 PARi whereas Rao and
Mendham (1991) calculated RUEi values from 2.71 to 3.5 g MJ−1 PARi and, before flowering,
Mendham and Salisbury (1995) used the value of 3.5 g MJ−1 PARi in the EPIC model for the
aerial parts and 4.0 g MJ−1 PARi for the total
biomass (Kiniry et al., 1995). Concerning RUEa, large variations were also observed: Gosse et al. (1983) and Rode et al. (1983), for spring-sown oilseed rape, calculated a constant RUEa for the aerial parts at 2.19 g MJ−1 PARa until 21 days
after flowering, and then only 1.06 g MJ−1
PARa, whereas Leach et al. (1989) measured RUEa varying from 1.8 to 4 g MJ−1
PARa during the vegetative phase of winter rape, and about 4 g MJ−1 PARa during the post-flowering
stage. Likewise Habekotte´ (1996, 1997b) found important variations in RUEa (for ADM) be-tween the beginning of spring or near maturation (1.1 g MJ−1 PARa) and during the onset of
flowering (2.62 g MJ−1 PARa); she then
imple-mented RUEa according to the development
stage in the LINTUL-BRASNAP model
(Habekotte´, 1997a). This literature review illus-trates significant variations in RUEa, which make it questionable to select a single value, for in-stance for use in a crop simulation model for oilseed rape.
Several causes of variation in RUE due to physical factors of the crop environment or in-trinsic characteristics of oilseed rape have been suggested, such as the significant effect: (i) of extreme temperatures, either very low or very high (Mendham and Salisbury, 1995); (ii) of de-velopmental stage (Gosse et al., 1983; Rode et al., 1983; Leach et al., 1989), particularly in the post flowering phase due to the high energy cost of lipid compounds (Habekotte´, 1997a); (iii) of win-ter and spring sowing period (Gosse et al., 1986); (iv) of sowing density or number of plants per m2
(Morrison and Stewart, 1995); or (v) of water stress (Mendham and Salisbury, 1995; Andersen et al., 1996). However, other authors have not found any significant effect of temperature (Gosse et al., 1983; Rode et al., 1983; Habekotte´, 1996), or of the plant density per m2
(Habekotte´, 1996).
Moreover, causes of variation in RUE may be related to the method of calculation, notably due to failure to take account of: (i) large losses of leaf biomass during flowering which can even lead to negative RUE (Leach et al., 1989; Yates and Steven, 1987); or (ii) the ground cover ratio at the beginning of growth; this can explain the row width or year to year effects observed by Morrison and Stewart (1995).
If the effect of N on LAI expansion is well known and integrated in oilseed rape crop simula-tion models (DAISY model: Petersen et al., 1995; CERES model: Gabrielle et al., 1998b), the effect of N on RUE remains to be assessed, as far as oilseed rape is concerned. In fact, although Be´-langer et al. (1992) showed a large effect of N on RUE for tall fescue (Festica arundinaceaSchreber) pastures, Gosse et al. (1983) and Rode et al. (1983) only found a very small N effect on RUEa for spring rape, and Leach et al. (1989) and Andersen et al. (1996) did not find any relation between N fertilisation and RUEa or RUEi for
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winter rape, respectively. However, none of these authors quantified the actual N nutritional state of the crop. The N status of a crop may be assessed by using the N nutrition index (NNI) proposed by Lemaire and Gastal (1997). Be´langer et al. (1992) used the NNI successfully to take account of the effect of N on the RUEa of forage grasses. In the same way, Lemaire et al. (1997) shown that for maize RUEa was strongly reduced by N deficiency: the relationship between RUEa and NNI was linear for values of NNI between 0.5 and 1. This high sensitivity of RUEi to N deficiency was also observed by Muchow and Davis (1988) and Sinclair and Horie (1989) for maize, sorghum, rice and soybean. Until now there have been no studies on the variation of oilseed rape RUEa as a function of its N nutri-tion. Recently, Gabrielle et al. (1998a) proposed a CERES-Rape model including N stress on LAI and obtained significant over-estimation of DM for unfertilised crops; they hypothesised that RUEa decreased in response of N deficiency. Now, RUEa is a widely used parameter in crop simulation models; it seems then necessary to assess the magnitude of the N effect on it.
The objective of this work was to investigate the effect of N on the RUEa of winter oilseed rape canopies which had received different doses of N fertiliser, using the NNI. After having ac-counted for the influence of N status on RUEa, the effect of temperature for all development stages of the crop was also investigated, which enabled one to avoid confounding interactions between N and temperature. Moreover, to limit the influence of experimental artefacts, the RUEa was calculated on the basis of the radiation
ab-sorbed by the crop (which yielded RUEa), and by taking account the total biomass of the crop, including the measured dry matter of the leaves which fell onto the soil during growth (generated total dry matter).
2. Materials and methods
2.1. Field location, general design and treatments Data were collected from September 1994 to July 1995 in a field in the Champagne area (North-eastern France, 48°50% N, 2°15% E). The soil is a very calcareous rendosol consisting of a rendzina (0 – 28 cm layer) overlying chalky and loamy ‘cryoturbated’ material (28 – 120 cm layer); the chalk substratum is found below 120 cm. The main soil characteristics were described previously by Leviel et al. (1998).
A winter oilseed rape crop (Brassica napus c6 oleifera Metzg., cv Goe´land) was sown on 9 Sep-tember, 1994 and harvested on 11 July, 1995; the plant density was 60 plants m−2. Three N
treat-ments were applied: nil (treatment N0), subopti-mal split applications made in spring totalling 135 kg N ha−1
(treatment N135), and a high applica-tion of 272 kg N ha−1 applied in four doses
(treatment N270) (Table 1). The experiment was laid out as a split plot design, with N treatments as main plots and sampling dates as sub-plots. This arrangement was replicated in three blocks. Other fertilisation (P, K, Mg, S) was carried out at rates which ensured that there would be no deficiency. Phytosanitary protection was complete and effective. Meteorological data were
continu-Table 1
Dates and amounts of fertiliser applied to the three oilseed rape crops in kg N ha−1
Date (and development stage) Total
Treatment
15/03/95 29/03/95 12/09/94 20/02/95
(inflorescence formation) (16 leaves) (stem elongation)
(sowing)
0 0
0
N0 0 0
78 0
N135 57 0 135
272 38
107 78
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ously recorded on site: incoming radiation (R), air temperature, potential evapotranspiration, rain.
Linear and non-linear regression fittings were done using the REG and the NLIN procedures of the SAS software, respectively (SAS Institute Inc., 1987).
2.2. Plant measurements
At 17 dates throughout the growth of the crop (emergence to harvest) three plots of 0.435 m2
were sampled per block (two contiguous rows of 0.75 m length). Sampling frequency varied from 2 to 4 weeks, depending on growing conditions. Depending on which organs were present, each sample was separated into several fractions: roots (mainly taproots), stems, branches, green leaves, senescent leaves, dead leaves, inflorescences, and pods. Leaves were considered senescent when they were more than half discoloured, and dead when they were very easily detached from the axis. The ADM consisted of all the green and senescent aerial parts present on the plant. The mass of dead leaves falling on the soil was estimated by collecting the dry matter of the leaves which had fallen on the soil (DDM=dead DM), on previ-ously installed plastic mesh, twice a week throughout the growth period for all three treatments.
Also, by using core sampling of the soil, and washing out and weighing the root mass (RDM=root dry matter) was measured twice (in early spring and at flowering): the dry weight of fine roots was very small (B10%) by comparison with the taproot, and thus negligible. Hence the TDM was calculated by adding ADM+RDM, and the generated total dry matter (gTDM) was obtained by summing TDM with DDM for each sampling date.
The developmental stages of the crop were recorded using the INRA-CETIOM phenological scale (INRA-CETIOM, 1988).
Each of the plant fractions was dried at 80°C in a forced-draught oven to constant weight and then weighed. After grinding, the total N content was measured (Dumas method) for each fraction and the weighted average N content of the aerial parts was calculated.
2.3. Measurements of area indices
The areas of the leaves and pods were measured by planimetry (Li-Cor, Delta-T devices, or Ayashi Denko optical planimeter), with the lamina and petiole together. The green leaf area index (green LAI) was calculated as the ratio of measured leaf area to the area of soil sampled; the same was done for the pods (PAI for pod area index). The flower area index (FAI) was estimated as the product of the mean flower size and the number of flowers present per unit area of soil. The num-ber of flowers was calculated from day to day after counting the number of flowering axes (main stems and branches) and measuring the dynamics of flower generation and the mean lifespan of a flower. It was confirmed that the area of a single flower (area of four petals) is stable whatever the position of the flower in the canopy, and for all treatments, as already established by Yates and Steven (1987) and Habekotte´ (1997b); the value found for the cultivar Goe´land was 1.99 cm2
flower−1. The rate of flower production on the
main stem was measured at 17.2 flowers 100°C day−1
(base 0°C) and 24 flowers 100°C day−1
for N135 and N270, respectively; it was however less on the side branches: 12.8, 14.7 and 16.2 flowers 100°C day−1 for N0, N135 and 270 respectively. 2.4. Calculation of PAR absorbed by the canopy
As one wanted to estimate the efficiency of conversion of radiation absorbed by the green parts of the plant which were photosynthetically active (leaves and pods), the absorbed PAR (PARa) was calculated day by day for each layer of the green canopy (green LAI, PAI and FAI) following the three layers radiation balance scheme proposed by Chartier et al. (1983) (Fig. 1). The absorbed radiation (PARaX) of each
homo-geneous layer X was calculated using a form of Beer’s Law, as follows:
PARaX=PARX×(1−rX)×[1−e
(−KX×XAI)]
(1) Where PARXis the radiation incident on the layer
X, rX is the reflection coefficient of the layer X
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coeffi-Fig. 1. Crop radiation balance using a 3-layer model (adapted from Chartier et al., 1983).
below (or the soil). During flowering, this calcula-tion involves the calculacalcula-tion of the radiacalcula-tion reflected and transmitted by flowers; the calcula-tion was made using the method proposed by Habekotte´ (1997b), taking account of two spectral bands: a (400 – 525 nm) and b (525 – 700 nm). Only first-order reflections are considered. The calcula-tion was made for each day, from daily incoming radiation for the day and canopy LAI, with the latter linearly interpolated between sampling dates. The values of the various parameters in-volved are shown in Table 2. The photosyntheti-cally active radiation (PAR) was estimated as 50% of the total incoming radiation (R) measured on the site (Varlet-Grancher et al., 1989).
The cumulative PARa for the three layers (PARa) was calculated on a daily basis for the time interval between two sampling dates, which required to interpolate LAI and PAI between these two dates. In view of the quite frequent samplings, linear interpolation was used, based on degree-days with a base of 4.5°C (Gabrielle et al., 1998b).
Given that the row arrangement of the crop influences radiation interception at the beginning of growth (LAI51.5), the ground cover ratio was cient, and XAI is the index for the layer (AI=
area index, m2m−2). The subscriptXcorresponds
to: L for green LAI, P for PAI and F for FAI. The incident radiation PARX is the sum of the
radiation transmitted by the layer above (or the atmosphere) and that reflected from the layer
Table 2
Value and references of parameters used in the calculation of the radiative balance for each layer of the oilseed rape cropa
References Parameter
Layer Value of parameter
0.772 Kfa
Kf
FAI Habekotte´ (1997b)
Kfb 0.506
Andersen et al. (1996)
PAI Kp 0.5
Mean of references values from:
LAI Kl 0.75
Mendham and Salisbury (1995) 0.5–0.6
Morrison and Stewart (1995) 0.65
0.71 Child and Butler (1987) cited by Hough (1990) Chartier et al. (1983)
0.85
0.903 Habekotte´ (1997b)
rl or rp 0.05
LAI and PAI (canopy level) Mean of references values from: 0.047 Yates and Steven (1987) 0.03–0.06 Leach et al. (1989)
rf rfa
FAI (organ level) 0.035 Habekotte´ (1997b)
rfb 0.45 (for PAR spectral band a or b)
tfa
tf 0.035
tfb 0.15
rs Cellier et al. (1996)
Soil 0.2
aSignificance of parameters: K=extinction coefficient,r=reflection coefficient (or albedo);t=transmission coefficient. See text
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taken into account (Chartier et al., 1983). Thus, to account for the variation in ground cover until the stem elongation phase, an effective index of ground cover was introduced to estimate the in-tercepted radiation (Jones, 1992), and Eq. (1) was applied within the row. The LAI, measured over the whole plot, was thus related to the fraction occupied by the row within the plot, according to a formula derived from Eq. (1):
PARaL=GCR×PARL×(1−rL)
×{1−e[−KL×(LAI/GCR)]} (2)
where GCR is the ground cover ratio (unitless). The ground cover ratio was estimated for the eight first sampling dates, from numerical treat-ment of digitised picture taken at a 1.5 m height above the ground. Between measurements, the GCR was interpolated using a regression of LAI on GCR obtained from the sampling dates.
2.5. Calculation of RUEa
In principle, RUEa may be calculated between two successive sampling dates as the ratio of crop dry matter production to total absorbed PAR over the corresponding time period. Here, dry matter production was calculated from the changes in generated dry matter (gTDM), as de-scribed in the ‘plant measurements’ section. Al-though the measurements of gTDM were quite precise (CVsB15%), the RUEa values thus ob-tained were affected by a significant random vari-ation, with a saw-tooth pattern. This may be explained by errors propagating from one time interval to the next. For instance, if gTDM was under-estimated on one sampling date, then RUEa was accordingly under-estimated on the time interval preceding this sampling, and over-es-timated on the following time interval. In order to smooth this variability, one chose to estimate RUEa over longer time periods spanning two to three sampling dates, and corresponding to differ-ent developmdiffer-ent stages. Here, RUEa was taken as the slope of the linear regression (unconstrained) between cumulative gTDM production and ab-sorbed PAR, over these time intervals.
2.6. Calculation of NNI
The N nutritional status for each treatment was quantified using the NNI (Lemaire and Gastal, 1997) which is calculated as follows:
NNI=Nm/Nc (3)
where Nm is the measured total N concentration for all the aerial parts and Nc is the critical total N concentration calculated for the value of ADM measured in situ; Nm and Nc are expressed as % of ADM. Nc is the minimum N concentration needed to obtain the maximum dry matter pro-duction by the crop. Nc is regarded as constant for low biomasses, and subsequently drops as ADM increases, according to a relationship known as ‘N dilution’. It can be used for a large number of herbaceous species: wheat, maize, for-age grasses, lucerne, peas, barley, durum wheat, sorghum etc. Although N dilution is a general phenomenon, parameters of the critical N dilution curve must be determined for each crop species (Lemaire and Gastal, 1997). Nc has been estab-lished for oilseed rape by Colnenne et al. (1998) from juvenile stages up to flowering, correspond-ing to values of ADM from 0.2 to 6.3 t ha−1:
Nc=4.63 if ADM50.88 t ha−1 (4a)
Nc=4.48×ADM−0.25
otherwise (4b)
NNI was calculated for each sampling date and was then averaged for the period of two to three measurement dates corresponding to the calcula-tion of RUEa as a funccalcula-tion of development stage. A value of NNI]1 indicates a crop with ample
N supply (N non-limiting); NNI=1 represents optimal N nutrition. The more NNI falls below 1, the more deficient is the crop in N.
3. Results
3.1. Changes in NNI o6er time
Table 3 shows the changes in NNI in relation to developmental stage for the three treatments. The NNI was far greater than unity at the begin-ning of growth for all the treatments, showing
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Table 3
Mean air temperature (°C), RUEa (g MJ−1 PARa) and nitrogen nutrition index (NNI) of the three treatments for each
developmental stage
Radiation use efficiency
Mean air temperature NNI
Oilseed rape stages
N0 N135 N270 N0 N135 N270
1.13 1.11
B1 to B5 (early Autumn growth) 11.3 1.14 1.16
(0.03) (0.05) (0.06) (0.07)
2.45 2.93 0.92
B6 to B11 (Autumn growth) 9.9 1.13
(0.09) (0.19) (0.09) (0.08)
0.74 0.98
B12 to B16 (Winter growth) 4.9a 0.73 1.01
(0.06) (0.10) (0.01)
(Frost period) (0.04)
5.8
C1 to C2 (Spring stem elongation) 1.75 1.61 2.17 0.72 0.80 1.06 (0.04) (0.15) (0.16) (0.01) (0.09) (0.06) 6.8
D1 to D2 (inflorescence formation) 1.80 2.78 2.69 0.64 1.10 1.29 (0.22) (0.07) (0.18) (0.07) (0.08) (0.08) 2.52 3.38 3.90
10.8 0.50
F1 to G2 (flowering) 0.83 1.20
(0.06) (0.08) (0.12) (0.02) (0.09) (0.10) 1.95 2.27 3.40
12.4 0.37b
G3 to G4 (pod formation) 0.56b 0.92b
(0.07) (0.15) (0.26) (0.04) (0.08) (0.11) 0.42 0.48 0.52
16.9 G5 to maturity (ripening)
(0.09) (0.07) (0.08)
aMean air temperature for the period using mean daily values (including negative values).
bNNI calculated with an extrapolation of the critical dilution curve beyond flowering (Colnenne et al., 1998).
Numbers in brackets corresponds to the standard error of RUEa and NNI.
that early growth was not limited by N, even when no fertiliser was applied at sowing (N135 and N0 treatments). Thereafter, the course of NNI differed across treatments: (i) it remained above 1 for N270, confirming that this treatment was non-limiting in N until the end of flowering; (ii) it fell steadily throughout the whole growth period for N0, indicating a progressive increase in N deficiency, which proved considerable by the time of flowering; and (iii) varied as a result of the two spring applications of N for treatment N135. For the latter, N deficiency appeared and devel-oped from the pod formation stage (stage G2) onwards, implying that the N135 dose did not sustain maximum growth after flowering.
As the N270 treatment was always non-limiting in N, it was assumed to have achieved the maxi-mum RUEa as proposed by Be´langer et al. (1992) for tall fescue swards, also bearing in mind that possible limitations set by other nutrients, or fungal diseases or insects were completely allevi-ated.
3.2. Green LAI, PAI and FAI changes o6er time The changes in green LAI, PAI and FAI ac-cording to thermal-time (basis 4.5°C) or develop-ment stage are shown in Fig. 2. LAI increase was approximately exponential and then linear in au-tumn. In winter time, a frost period at the begin-ning of January caused green leaves to drop from the base of the canopy, and LAI decreased. From the end of winter to flowering, green LAI in-creased again linearly, after which it declined very rapidly to reach 0 at harvest.
The maximum PAI was reached at the end of pod formation (G4 stage), when it amounted to 2.6 m2
m−2
for N270. This high value illustrates the importance of including it when calculating the crop PARa.
The development of FAI, which depends on the duration of flowering (ca. 1 month), was very sporadic. However the maximum FAI was 0.55 m2 m−2 for N270, which justifies including it in
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N had a very large effect on the morphogenesis of oilseed rape since the N deficiencies achieved with N0 and to a lesser extent with N135 caused a very clear decrease in green LAI and also in PAI and FAI comparing to N270.
3.3. PAR assessment for each layer of the canopy As the values of green LAI and PAI were significantly less for N0 and N135 than for N270, the sum of PARa (PARa) absorbed by the green LAI and PAI was significantly different between the three treatments (Fig. 3a). At harvest, the PARa absorbed by the sole green LAI was 765, 683 and 521 MJ m−2 for N270, N135 and N0
respectively; when including the pods thePARa became substantially larger, at 1129, 1001 and 766 MJ m−2 for N270, N135 and N0, respectively.
Fig. 3. Calculated cumulative absorbed photosynthetically ac-tive radiation (PAR): by green LAI and PAI (a), FAI and soil (b), and cumulative reflected PAR from the canopy and soil (c) vs. thermal-time from emergence (and development stage) for the three N treatments.
Fig. 2. Measured green LAI (a), PAI (b), and FAI (c) vs. thermal-time from emergence (and development stage) for the three N treatments. (Bars represent S.E.).
Conversely, the PAR absorbed by the soil and that reflected by the crop (unused for photosyn-thesis) were higher for N0 and N135 than for N270 (Fig. 3b,c). Neither the amount of PAR absorbed by the FAI (range: 40 – 60 MJ m−2), nor
the one reflected by the crop (range: 112 – 163 MJ m−2
) were negligible (Fig. 3c).
3.4. ADM, DDM and gTDM changes o6er time The evolution of the different biomass fractions measured on the three treatments according to thermal-time or development stage is shown in Fig. 4. The dynamics of the accumulation of ADM were similar to those obtained for green LAI, namely: (i) at first, exponential growth; (ii)
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next a fall in ADM resulting from leaf fall in winter; (iii) linear growth after the end of winter until the end of flowering; and lastly (iv) very slow or zero growth at the end of the growing period (Fig. 4a). The amount of estimated dead DM (DDM) was very large at 480 g m−2 for N270 at
the end of season (Fig. 4b). Estimates of DDM were consistent with the rest of the DM since positive variations were always obtained when calculating the generated TDM (gTDM), despite heavy leaf falls in winter (Fig. 4c). The amount of gTDM produced was very large for N270, being 2347 g m−2
at harvest. Also, as with green LAI, there was a strong effect of N on DM production with a reduction in gTDM of 51% for N0 and 22% for N135 (Fig. 4c). This resulted in
signifi-cant yield losses: 5.36 t ha−1 of grains were
produced for N270 compared to only 4.54 and 3.07 t ha−1 for N135 and N0, respectively
(Gabrielle et al., 1998a).
3.5. Variation in RUEa
Table 3 lists the values and standard errors of calculated RUEa, for different development stages, along with gTDM and PARa for LAI and PAI. The RUEa significantly varied with the development stage and also with the N treatment, from 0.74 to 3.90 g MJ−1
. It was also found that the RUEa on treatment N270 was always signifi-cantly greater than on treatments N0 and N135 when their NNI was less than 1 (N deficiency), confirming the effect of N on RUEa in a situation of N deficiency. On the other hand the RUEa was the same for all treatments when NNI was above 1 (N non-limiting situation). However, as the RUEa varied much more with the development stage than between the other two N treatments, there was no strict single relationship between RUEa and NNI (Table 3). Thus, to remove any effect other than crop N status (NNI value) on the RUEa, the ratio of actual to maximum RUE (RUEa/RUEamax) was calculated for each
devel-opment stage, as proposed by Be´langer et al. (1992) for tall fescue swards fertilised with differ-ent rates of N. Since the NNI of the N270 treat-ment was always ]1 (N non limiting) until flowering, it was assumed that the maximum RUEa (RUEamax) was always obtained for the
N270 treatment. Consequently, by definition, RUEa/RUEamaxwas always equal to 1 for N270.
Fig. 5 shows the relationship between NNI and RUEa/RUEamax for the other two N treatments,
when NNIB1. A close relationship was obtained between NNI and the RUEa ratio showing a sharp decrease of RUEa from a NNI value of ca. 1 – 0.4. A linear regression yielded a good fit of the response of RUEa to N deficiency:
RUEa/RUEamax=0.74×NNI+0.23 (5) Statistical indicators were satisfactory: RMSE=0.028 g MJ−1 PARa and r2=0.919 (8
d.f.).
Fig. 4. Measured aerial dry matter (ADM) (a), cumulative dead DM (b), and generated total dry matter (gTDM) (c) vs. thermal-time from emergence (and developmental stage) for the three N treatments. (Bars represent S.E.).
(10)
Fig. 5. Relationship between nitrogen nutrition index (NNI) and RUEa/RUEamax. (Bars represent S.E.).
However, since the NNI value of N270 was not
]1 after the pod formation stage, Eq. (6) was
used to calculate an estimate of RUEamax at this
later stage for the treatment N270. Fig. 6 shows the relationship between periodic mean air tem-perature (T) and RUEamaxfor stages B6 (6 leaves)
to G1 (beginning of pod formation). A significant relationship was obtained between temperature and RUEamax; the following exponential model
gave a satisfactory fit to the data: RUEamax=3.5×[1−13.1×e(0.6×T)
] (6)
Statistical indicators were acceptable: RMSE=
0.27 g MJ−1
PARa;r2
=0.907 (4 d.f.). This may be considered as an approximation of the temper-ature effect on RUEa for oilseed rape. However, this clearly shows that below a given threshold (6 – 7°C) the RUEa was dramatically reduced. On the other hand, the temperature does not explain the low value of RUEamax at early stages after
emergence (B1 – B5 leaves) or during the ripening stage.
4. Discussion
4.1. The ad6antage of using generated TDM and PARa to calculate RUEa
The mean RUEa over the whole crop cycle (excluding the end of ripening) was 1.76, 2.34 and 2.63 g MJ−1 PARa for N0, N135 and N270,
respectively. When calculated from TDM (exclud-ing dead DM), then mean RUEa was ca. 20% less: 1.38, 1.88 and 2.17 g MJ−1 PARa for N0,
N135 and N270, respectively. Thus, including dead DM ensured that the calculated RUEa is always positive especially after periods of severe winter frost (as occurred here in January), and should avoid misinterpretation of the data.
The maximum theoretical yield of photosynthe-sis (RUEa calculated as energy equivalent) is in the order of 5 g MJ−1 PARa (Russell et al.,
1989). The maximum values obtained in this work were substantially lower: 3.9 g TDM MJ−1PARa
for N270 at flowering, despite the inclusion of DDM. However the values of RUEamaxobtained
in this work are similar to the value of 4.0 g
Fig. 6. Relationship between periodic mean air temperature and RUEamaxfrom emergence until flowering (Bars represent
S.E.).
In a second step, the apparent effect of develop-ment stage on RUEa was investigated, by relating it to mean air temperature over each period (see Table 3). In order to alleviate interactions with N, only the RUEa values corresponding to a NNI greater than unity were used (N non-limiting situ-ations, which entailed RUEa equal RUEamax).
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MJ−1 PARi used by Kiniry et al. (1995) in the
EPIC model (aerial parts plus roots) and that of 4 g MJ−1 PARa observed by Leach et al. (1989)
during the post-flowering stage of winter rape. Calculation of RUE using PARi instead of PARa gives lower values of RUEi, on average about 13% lower than the RUEa values (results not shown). This is explained by the large propor-tion of PAR which is reflected by the crop (partic-ularly during flowering) and the soil (Varlet-Grancher et al., 1989).
4.2. Effect of N on RUEa
Andersen et al. (1996) did not show a signifi-cant effect of N on RUEi for oilseed rape. How-ever, an effect of N on RUEa was observed in the experiment; this is in good agreement with the results obtained by Be´langer et al. (1992) for tall fescue swards and Lemaire et al. (1997) for maize. Be´langer et al. (1992) showed that the ratio RUEa/RUEamax is very closely correlated with
NNI according to a monomolecular equation; however this kind of function does not improve the relationship between RUEa/RUEamax and
NNI in this study, so a linear regression has been used.
It should be emphasised that with this regres-sion (Eq. (5)), RUEa stops increasing as soon as NNI exceeds unity, which is in accordance with the results of Lemaire et al. (1997). The effect of N on RUEi has already been shown for maize, rice and soybean by Muchow and Davis (1988) and Sinclair and Horie (1989) for maize, sorghum, rice and soybean, who related it to the concentra-tion of N per unit area of leaves. Their response curves were curvilinear, and RUEi changed little for leaf N contents above 2 g m2.
4.3. Effect of temperature on RUEa
These results suggest a dependency of RUEamax
on mean air temperature, in agreement with the results of Andrade et al. (1993) and Verheul et al. (1996) for maize. On the other hand, Habekotte´ (1996) did not find any effect of temperature on RUE, but her measurements were made at later stage (after inflorescence formation, probably
when the mean air temperature was high). The optimum temperature for photosynthesis in rape is about 20 – 25°C (Gosse et al., 1983; Paul et al., 1990), with a small linear increase in gross assimi-lation from 6 to 20°C and no increase from 20 to 30°C (Paul et al., 1992). The optimum seems to vary according to the growing conditions of the rape (a plant acclimation phenomenon). Thus, Gosse et al. (1983) and Rode et al. (1983) found only a small temperature effect on leaf photosyn-thesis per unit area over the range 14 – 28°C. The results obtained here seem compatible with the latter, since RUEamax is slightly reduced from 12
to 6 – 7°C, and strongly depressed below a threshold of about 6 – 7°C (Fig. 6). Lastly, there remains a clear effect of development stage on RUEamaxfor the early rosette stages (1 – 6 leaves)
and late (end of pod formation until harvest) stages (Table 3).
4.4. Effect of de6elopment stage on RUEa
Variations in RUEa with developmental stage have also been found by Gosse et al. (1983), Rode et al. (1983), Leach et al. (1989), and Habekotte´ (1996, 1997b). In these cases, the variation in RUEa occurred mainly in the post flowering phase when it is attributable to the formation of lipid compounds with a high energy cost, whereby more radiation is required to achieve the same TDM gain (Habekotte´, 1997b). Hence, for late growth stages, the RUE calculated by taking ac-count of the energetic value of the biochemical compounds is about 1 g MJ−1 PARa, as against
a maximum of 3.6 g MJ−1 at the beginning of
flowering (Habekotte´, 1997b). This lower value of RUEa at the end of the growing period could also partly be explained by a lower photosynthetic capacity of stems and pods, compared to leaves, which also declines over the course of time. In fact the net assimilation rate per unit area of flower stems and peduncles would be 25% less, and that of pods 75% less than that of leaves (Rode et al., 1983).
As far as the low value of RUEa at the begin-ning of growth is concerned, this could be ex-plained by a smaller leaf photosynthetic capacity and perhaps by a saturated leaf photosynthesis
(12)
rate which is reached more quickly at a low level of green LAI; this however remains to be verified.
5. Conclusion
This RUEa of winter oilseed rape allowed to obtain actual estimates through adopting a de-tailed radiation balance and continuously moni-toring dead biomass. The latter resulted from leaf drop, which occurred at a significant rate throughout the growth period, and is known to cause artefacts in the calculation of RUEa when ignored. Next, it was able to relate the large seasonal variations of RUE to three main factors, namely: mean air temperature, development stage, and crop N nutrition status. By quantifying the latter with the NNI, it could be possible to sepa-rate the effect of N from that of other factors. NNI proved to be directly correlated with the ratio RUEa/RUEamaxin cases with N deficiency.
As regards the other two factors, temperature explained a large part of the apparent effect of development stage on RUEa, so that it was only during the very early and late stages that RUEa appeared to be affected by crop ontogeny. It has been shown that N deficiency in oilseed rape crops affects: (i) primarily green LAI and PAI, and hence the cumulative PAR absorbed by the crop; but also (ii) RUEa by probably decreasing the efficiency of photosynthesis per photosyn-thetic unit. Thus, as concluded by Be´langer et al. (1992) for gramineous species, the effect of N on oilseed rape gTDM production at the canopy level actually lumps the effect of N deficiency on physiological processes (photosynthesis per unit area) and on morphological processes (leaf elon-gation rates), with the latter influencing absorbed PAR. Both effects may be quantitatively related to crop NNI, as shown here for RUEa and by Gabrielle et al. (1998b) for LAI.
The relationships proposed here to express the effects of N and air temperature on RUEa, which are a first experimental estimation, should be fur-ther validated under a broader range of weafur-ther conditions and sowing dates. However, they may readily be expected to improve the accuracy of crop simulation models, such as the CERES-rape
model (Gabrielle et al., 1998a) in which they are to be implemented.
Acknowledgements
The authors would like to thank G. Alavoine, M-J. Herre, S. Millon, F. Million and P. Thie´beau (INRA Reims), M. Lauransot and B. Leviel (INRA Grignon) for their technical assistance. The authors are also indebted to ADEME, INRA (AIP Ecofon) and CETIOM who supported this program. We thank Dr A. Scaife for translating this manuscript into English.
References
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Andersen, M., Heidman, T., Plauborg, F., 1996. The effects of drought and N on light interception, growth and yield of winter oilseed rape. Acta Agric. Scand. Sect. B Soil Plant Sci. 46, 55 – 67.
Be´langer, G., Gastal, F., Lemaire, G., 1992. Growth analysis of a tall fescue sward fertilized with different rates of nitrogen. Crop Sci. 32, 1371 – 1376.
Cellier, P., Richard, G., Robin, P., 1996. Partition of sensible heat fluxes into bare soil and the atmosphere. Agric. For. Meteor. 82, 245 – 265.
Chartier, M., Fabre, B., Gosse, G., Rode, J.C., 1983. Bilan radiatif d’un couvert de colza. Actes du 6e`me Congre`s International sur le Colza, 17-18-19/5/1983, Paris, tome 1, pp. 154 – 165.
Colnenne, C., Meynard, J.M., Reau, R., Justes, E., Merrien, A., 1998. Determination of a critical nitrogen dilution curve for winter oilseed rape. Ann. Bot. 81, 311 – 317. Gabrielle, B., Denoroy, P., Gosse, G., Justes, E., Andersen,
M., 1998. Development and evaluation of a CERES-type model for winter oilseed rape. Field Crops Res. 57, 95 – 111.
Gabrielle, B., Denoroy, P., Gosse, G., Justes, E., Andersen, M., 1998. A model of leaf area development and senes-cence for winter oilseed rape. Field Crops Res. 57, 209 – 222.
Gosse, G., Rollier, M., Rode, J.C., Chartier, M., 1983. Vers une modelisation de la production chez le colza de print-emps. Actes du 6eme Congre`s International sur le Colza, 17-18-19/5/1983, Paris, tome 1, pp. 116 – 123.
Gosse, G., Varlet-Grancher, C., Bonhomme, R., Chartier, M., Allirand, J.-M., Lemaire, G., 1986. Production maximale de matie`re se`che et rayonnement solaire intercepte´ par un couvert ve´ge´tal. Agronomie 6, 47 – 56.
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Habekotte´, B., 1996. Winter oilseed rape. Analysis of yield formation and crop type design for higher yield potential. Ph.D Thesis, Wageningen Agricultural University, p. 156. Habekotte´, B., 1997. A model of the phenological develop-ment of winter oilseed rape (Brassica napus L.). Field Crops Res. 54, 127 – 136.
Habekotte´, B., 1997. Evaluation of seed yield determining factors in winter oilseed rape under potential growth con-ditions (Brassica napusL.) by means of crop growth mod-elling. Field Crops Res. 54, 137 – 151.
Hough, M.N., 1990. Agrometoerological aspects of crops in the United Kingdom and Ireland. A review for sugar beet, oilseed rape, peas, wheat, barley, oats, potatoes, apples and pears. An agricultural information system for the Eu-ropean Community, Report EUR 13039 EN, Joint Re-search Centre, ISPRA.
INRA-CETIOM, 1988. Colza, physiologie et e´laboration du rendement. Information Technique CETIOM, supplement no. 103, Paris, p. 158.
Jones, H.G., 1992. Plants and Microclimate. A Quantitative Approach to Environmental Plant Physiology. Cambridge University Press, Cambridge, p. 428.
Kiniry, J.R., Major, D.J., Izaurralde, R.C., Williams, J.R., Gasman, P.W., Morrison, M., 1995. EPIC model parame-ters for cereal, oilseed rape and forage crops in the north-ern Great Plains region. Can. J. Plant Sci. 75, 679 – 688. Leach, J.E., Milford, G.F.J., Mullen, L.A., Scott, T.,
Steven-son, H.J., 1989. Accumulation of dry matter in oilseed rape crops in relation to the reflection and absorption of solar radiation by different canopy structures. Aspect Appl. Biol. 23, 117 – 123.
Lemaire, G., Gastal, F., 1997. N uptake and distribution in plant canopies. In: Lemaire, G. (Ed.), Diagnosis of the Nitrogen Status in Crops. Springer-Verlag, Berlin, pp. 3 – 43.
Lemaire, G., Gastal, F., Ple´net, D., 1997. Dynamics of N uptake and N distribution in plant canopies. Use of crop N status index in crop modelling. In: Lemaire, G., Burns, I. (Eds.), Diagnostic Procedures for Crop N Management, Poitiers (France), 22 – 23 November 1995, INRA Editions, Paris, pp. 15 – 29.
Leviel, B., Gabrielle, B., Justes, E., Mary, B., Gosse, G., 1998. Water and nitrate budgets in a rendzina cropped with oilseed rape receiving varying amounts of fertilizer. Eur. J. Soil Sci. 49, 37 – 51.
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Mendham, N.J., Shipway, P.A., Scott, R.K., 1981. The effects of delayed sowing and weather on growth, development and yield of winter oilseed rape (Brassica napus). J. Agric. Sci. Camb. 96, 389 – 416.
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Paul, M.J., Lawlor, D.W., Driscoll, S.P., 1990. The effect of temperature on photosynthesis and carbon fluxes in sunflower and rape. J. Exp. Bot. 41 (226), 547 – 555. Paul, M.J., Driscoll, S.P., Lawlor, D.W., 1992. Sink-regulation
of photosynthesis in relation to temperature in sunflower and rape. J. Exp. Bot. 43 (247), 147 – 153.
Petersen, C., Jorgensen, U., Svendsen, H., Hansen, S., Jensen, H., Nielsen, N., 1995. Parameter assessment for simulation of biomass production and N uptake in winter rapeseed. Eur. J. Agron. 4, 77 – 89.
Rao, M.S.S., Mendham, N.J., 1991. Soil-plant water relations of oilseed rape (Brassica napusandBrassica campestris). J. Agric. Sci. Camb. 117, 197 – 205.
Rode, J.C., Gosse, G., Chartier, M., 1983. Vers une modelisa-tion de la producmodelisa-tion de graines de colza de printemps. Informations Techniques CETIOM 82, 10 – 20.
Russell, G., Jarvis, P.G., Monteith, J.L., 1989. Absorption of radiation by plant canopies and stand growth. In: Russell, G., Marshall, B., Jarvis, P.G. (Eds.), Plant Canopies: Their Growth, Form and Function, Soc. Exp. Bot., Seminar Series 31. Cambrige University Press, Cambridge, pp. 21 – 40.
SAS Institute Inc., 1987. SAS/STAT™ Guide for Personal Computers, Version 6 Edition. SAS Institute Inc., Cary, NC, p. 1028.
Sinclair, T.R., Horie, T., 1989. Leaf nitrogen, photosynthesis and crop radiation use efficiency: a review. Crop Sci. 29, 90 – 98.
Varlet-Grancher, C., Gosse, G., Chartier, M., Sinoquet, H., Bonhomme, R., Allirand, J.-M., 1989. Mise au point: rayonnement solaire absorbe´ ou intercepte´ par un couvert ve´ge´tal. Agronomie 9, 419 – 439.
Verheul, M.J., Picatto, C., Stamp, P., 1996. Growth and development of maize (Zea maysL.) seedlings under chill-ing conditions in the field. Eur. J. Agron. 5, 31 – 43. Yates, D.J., Steven, M.D., 1987. Reflection and absorption of
solar radiation by flowering canopies of oil-seed rape (Brassica napusL.). J. Agric. Sci. Camb. 109, 495 – 502.
. .
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N had a very large effect on the morphogenesis of oilseed rape since the N deficiencies achieved with N0 and to a lesser extent with N135 caused a very clear decrease in green LAI and also in PAI and FAI comparing to N270.
3.3. PAR assessment for each layer of the canopy As the values of green LAI and PAI were significantly less for N0 and N135 than for N270, the sum of PARa (PARa) absorbed by the green LAI and PAI was significantly different between the three treatments (Fig. 3a). At harvest, the
PARa absorbed by the sole green LAI was 765, 683 and 521 MJ m−2 for N270, N135 and N0
respectively; when including the pods thePARa became substantially larger, at 1129, 1001 and 766 MJ m−2 for N270, N135 and N0, respectively.
Fig. 3. Calculated cumulative absorbed photosynthetically ac-tive radiation (PAR): by green LAI and PAI (a), FAI and soil (b), and cumulative reflected PAR from the canopy and soil (c) vs. thermal-time from emergence (and development stage) for the three N treatments.
Fig. 2. Measured green LAI (a), PAI (b), and FAI (c) vs. thermal-time from emergence (and development stage) for the three N treatments. (Bars represent S.E.).
Conversely, the PAR absorbed by the soil and that reflected by the crop (unused for photosyn-thesis) were higher for N0 and N135 than for N270 (Fig. 3b,c). Neither the amount of PAR absorbed by the FAI (range: 40 – 60 MJ m−2), nor
the one reflected by the crop (range: 112 – 163 MJ m−2
) were negligible (Fig. 3c).
3.4. ADM, DDM and gTDM changes o6er time The evolution of the different biomass fractions measured on the three treatments according to thermal-time or development stage is shown in Fig. 4. The dynamics of the accumulation of ADM were similar to those obtained for green LAI, namely: (i) at first, exponential growth; (ii)
(2)
next a fall in ADM resulting from leaf fall in winter; (iii) linear growth after the end of winter until the end of flowering; and lastly (iv) very slow or zero growth at the end of the growing period (Fig. 4a). The amount of estimated dead DM (DDM) was very large at 480 g m−2 for N270 at
the end of season (Fig. 4b). Estimates of DDM were consistent with the rest of the DM since positive variations were always obtained when calculating the generated TDM (gTDM), despite heavy leaf falls in winter (Fig. 4c). The amount of gTDM produced was very large for N270, being 2347 g m−2
at harvest. Also, as with green LAI, there was a strong effect of N on DM production with a reduction in gTDM of 51% for N0 and 22% for N135 (Fig. 4c). This resulted in
signifi-cant yield losses: 5.36 t ha−1 of grains were
produced for N270 compared to only 4.54 and 3.07 t ha−1 for N135 and N0, respectively
(Gabrielle et al., 1998a).
3.5. Variation in RUEa
Table 3 lists the values and standard errors of calculated RUEa, for different development stages, along with gTDM and PARa for LAI and PAI. The RUEa significantly varied with the development stage and also with the N treatment, from 0.74 to 3.90 g MJ−1
. It was also found that the RUEa on treatment N270 was always signifi-cantly greater than on treatments N0 and N135 when their NNI was less than 1 (N deficiency), confirming the effect of N on RUEa in a situation of N deficiency. On the other hand the RUEa was the same for all treatments when NNI was above 1 (N non-limiting situation). However, as the RUEa varied much more with the development stage than between the other two N treatments, there was no strict single relationship between RUEa and NNI (Table 3). Thus, to remove any effect other than crop N status (NNI value) on the RUEa, the ratio of actual to maximum RUE (RUEa/RUEamax) was calculated for each
devel-opment stage, as proposed by Be´langer et al. (1992) for tall fescue swards fertilised with differ-ent rates of N. Since the NNI of the N270 treat-ment was always ]1 (N non limiting) until flowering, it was assumed that the maximum RUEa (RUEamax) was always obtained for the
N270 treatment. Consequently, by definition, RUEa/RUEamaxwas always equal to 1 for N270.
Fig. 5 shows the relationship between NNI and RUEa/RUEamax for the other two N treatments,
when NNIB1. A close relationship was obtained between NNI and the RUEa ratio showing a sharp decrease of RUEa from a NNI value of ca. 1 – 0.4. A linear regression yielded a good fit of the response of RUEa to N deficiency:
RUEa/RUEamax=0.74×NNI+0.23 (5)
Statistical indicators were satisfactory: RMSE=0.028 g MJ−1 PARa and r2=0.919 (8
d.f.). Fig. 4. Measured aerial dry matter (ADM) (a), cumulative
dead DM (b), and generated total dry matter (gTDM) (c) vs. thermal-time from emergence (and developmental stage) for the three N treatments. (Bars represent S.E.).
(3)
Fig. 5. Relationship between nitrogen nutrition index (NNI) and RUEa/RUEamax. (Bars represent S.E.).
However, since the NNI value of N270 was not
]1 after the pod formation stage, Eq. (6) was
used to calculate an estimate of RUEamax at this
later stage for the treatment N270. Fig. 6 shows the relationship between periodic mean air tem-perature (T) and RUEamaxfor stages B6 (6 leaves)
to G1 (beginning of pod formation). A significant relationship was obtained between temperature and RUEamax; the following exponential model
gave a satisfactory fit to the data: RUEamax=3.5×[1−13.1×e
(0.6×T)
] (6)
Statistical indicators were acceptable: RMSE= 0.27 g MJ−1
PARa;r2
=0.907 (4 d.f.). This may be considered as an approximation of the temper-ature effect on RUEa for oilseed rape. However, this clearly shows that below a given threshold (6 – 7°C) the RUEa was dramatically reduced. On the other hand, the temperature does not explain the low value of RUEamax at early stages after
emergence (B1 – B5 leaves) or during the ripening stage.
4. Discussion
4.1. The ad6antage of using generated TDM and PARa to calculate RUEa
The mean RUEa over the whole crop cycle (excluding the end of ripening) was 1.76, 2.34 and 2.63 g MJ−1 PARa for N0, N135 and N270,
respectively. When calculated from TDM (exclud-ing dead DM), then mean RUEa was ca. 20% less: 1.38, 1.88 and 2.17 g MJ−1 PARa for N0,
N135 and N270, respectively. Thus, including dead DM ensured that the calculated RUEa is always positive especially after periods of severe winter frost (as occurred here in January), and should avoid misinterpretation of the data.
The maximum theoretical yield of photosynthe-sis (RUEa calculated as energy equivalent) is in the order of 5 g MJ−1 PARa (Russell et al.,
1989). The maximum values obtained in this work were substantially lower: 3.9 g TDM MJ−1PARa
for N270 at flowering, despite the inclusion of DDM. However the values of RUEamaxobtained
in this work are similar to the value of 4.0 g Fig. 6. Relationship between periodic mean air temperature
and RUEamaxfrom emergence until flowering (Bars represent
S.E.).
In a second step, the apparent effect of develop-ment stage on RUEa was investigated, by relating it to mean air temperature over each period (see Table 3). In order to alleviate interactions with N, only the RUEa values corresponding to a NNI greater than unity were used (N non-limiting situ-ations, which entailed RUEa equal RUEamax).
(4)
MJ−1 PARi used by Kiniry et al. (1995) in the
EPIC model (aerial parts plus roots) and that of 4 g MJ−1 PARa observed by Leach et al. (1989)
during the post-flowering stage of winter rape. Calculation of RUE using PARi instead of PARa gives lower values of RUEi, on average about 13% lower than the RUEa values (results not shown). This is explained by the large propor-tion of PAR which is reflected by the crop
(partic-ularly during flowering) and the soil
(Varlet-Grancher et al., 1989).
4.2. Effect of N on RUEa
Andersen et al. (1996) did not show a signifi-cant effect of N on RUEi for oilseed rape. How-ever, an effect of N on RUEa was observed in the experiment; this is in good agreement with the results obtained by Be´langer et al. (1992) for tall fescue swards and Lemaire et al. (1997) for maize. Be´langer et al. (1992) showed that the ratio RUEa/RUEamax is very closely correlated with
NNI according to a monomolecular equation; however this kind of function does not improve the relationship between RUEa/RUEamax and
NNI in this study, so a linear regression has been used.
It should be emphasised that with this regres-sion (Eq. (5)), RUEa stops increasing as soon as NNI exceeds unity, which is in accordance with the results of Lemaire et al. (1997). The effect of N on RUEi has already been shown for maize, rice and soybean by Muchow and Davis (1988) and Sinclair and Horie (1989) for maize, sorghum, rice and soybean, who related it to the concentra-tion of N per unit area of leaves. Their response curves were curvilinear, and RUEi changed little for leaf N contents above 2 g m2.
4.3. Effect of temperature on RUEa
These results suggest a dependency of RUEamax
on mean air temperature, in agreement with the results of Andrade et al. (1993) and Verheul et al. (1996) for maize. On the other hand, Habekotte´ (1996) did not find any effect of temperature on RUE, but her measurements were made at later stage (after inflorescence formation, probably
when the mean air temperature was high). The optimum temperature for photosynthesis in rape is about 20 – 25°C (Gosse et al., 1983; Paul et al., 1990), with a small linear increase in gross assimi-lation from 6 to 20°C and no increase from 20 to 30°C (Paul et al., 1992). The optimum seems to vary according to the growing conditions of the rape (a plant acclimation phenomenon). Thus, Gosse et al. (1983) and Rode et al. (1983) found only a small temperature effect on leaf photosyn-thesis per unit area over the range 14 – 28°C. The results obtained here seem compatible with the latter, since RUEamax is slightly reduced from 12
to 6 – 7°C, and strongly depressed below a threshold of about 6 – 7°C (Fig. 6). Lastly, there remains a clear effect of development stage on RUEamaxfor the early rosette stages (1 – 6 leaves)
and late (end of pod formation until harvest) stages (Table 3).
4.4. Effect of de6elopment stage on RUEa
Variations in RUEa with developmental stage have also been found by Gosse et al. (1983), Rode et al. (1983), Leach et al. (1989), and Habekotte´ (1996, 1997b). In these cases, the variation in RUEa occurred mainly in the post flowering phase when it is attributable to the formation of lipid compounds with a high energy cost, whereby more radiation is required to achieve the same TDM gain (Habekotte´, 1997b). Hence, for late growth stages, the RUE calculated by taking ac-count of the energetic value of the biochemical compounds is about 1 g MJ−1 PARa, as against
a maximum of 3.6 g MJ−1 at the beginning of
flowering (Habekotte´, 1997b). This lower value of RUEa at the end of the growing period could also partly be explained by a lower photosynthetic capacity of stems and pods, compared to leaves, which also declines over the course of time. In fact the net assimilation rate per unit area of flower stems and peduncles would be 25% less, and that of pods 75% less than that of leaves (Rode et al., 1983).
As far as the low value of RUEa at the begin-ning of growth is concerned, this could be ex-plained by a smaller leaf photosynthetic capacity and perhaps by a saturated leaf photosynthesis
(5)
rate which is reached more quickly at a low level of green LAI; this however remains to be verified.
5. Conclusion
This RUEa of winter oilseed rape allowed to obtain actual estimates through adopting a de-tailed radiation balance and continuously moni-toring dead biomass. The latter resulted from leaf drop, which occurred at a significant rate throughout the growth period, and is known to cause artefacts in the calculation of RUEa when ignored. Next, it was able to relate the large seasonal variations of RUE to three main factors, namely: mean air temperature, development stage, and crop N nutrition status. By quantifying the latter with the NNI, it could be possible to sepa-rate the effect of N from that of other factors. NNI proved to be directly correlated with the ratio RUEa/RUEamaxin cases with N deficiency.
As regards the other two factors, temperature explained a large part of the apparent effect of development stage on RUEa, so that it was only during the very early and late stages that RUEa appeared to be affected by crop ontogeny. It has been shown that N deficiency in oilseed rape crops affects: (i) primarily green LAI and PAI, and hence the cumulative PAR absorbed by the crop; but also (ii) RUEa by probably decreasing the efficiency of photosynthesis per photosyn-thetic unit. Thus, as concluded by Be´langer et al. (1992) for gramineous species, the effect of N on oilseed rape gTDM production at the canopy level actually lumps the effect of N deficiency on physiological processes (photosynthesis per unit area) and on morphological processes (leaf elon-gation rates), with the latter influencing absorbed PAR. Both effects may be quantitatively related to crop NNI, as shown here for RUEa and by Gabrielle et al. (1998b) for LAI.
The relationships proposed here to express the effects of N and air temperature on RUEa, which are a first experimental estimation, should be fur-ther validated under a broader range of weafur-ther conditions and sowing dates. However, they may readily be expected to improve the accuracy of crop simulation models, such as the CERES-rape
model (Gabrielle et al., 1998a) in which they are to be implemented.
Acknowledgements
The authors would like to thank G. Alavoine, M-J. Herre, S. Millon, F. Million and P. Thie´beau (INRA Reims), M. Lauransot and B. Leviel (INRA Grignon) for their technical assistance. The authors are also indebted to ADEME, INRA (AIP Ecofon) and CETIOM who supported this program. We thank Dr A. Scaife for translating this manuscript into English.
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