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Published in Agron. J. 96:601-607 (2004).
© American Society of Agronomy
677 S. Segoe Rd., Madison, WI 53711 USA

NITROGEN MANAGEMENT

Nitrogen Dilution Curves and Nitrogen Use Efficiency During Winter–Spring Growth of Annual Ryegrass

María A. Marino*,a, Arturo Mazzantib, Silvia G. Assueroa, François Gastalc, Hernán E. Echeverríab and Fernando Andradeb

a Facultad de Ciencias Agrarias (UNMdP), CC 276, (7620) Balcarce, Buenos Aires, Argentina
b Estación Experimental Agropecuaria Balcarce (INTA), Balcarce, Buenos Aires, Argentina
c Unité de Recherche Écophysiologie des Plantes Fourragères–INRA, 86600 Lusignan, France

* Corresponding author (mmarino{at}copetel.com.ar).

Received for publication October 1, 2001.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
For some species, mathematical models have been developed to describe tissue N dilution during crop growth and to estimate the plant N status applying the N nutrition index (NNI), the ratio between the actual tissue N concentration and the tissue N concentration needed to obtain the maximum instantaneous crop growth rate (critical tissue N concentration). The objectives of this work were (i) to obtain the critical N dilution curve (NDC) for annual ryegrass (Lolium multiflorum Lam.) corresponding to late winter and early spring growth, (ii) to compare it with NDCs obtained by other authors, (iii) to estimate the NNI for different levels of N fertilization, and (iv) to determine the apparent N use efficiency (NUE) and its components: N uptake efficiency (NUpE) and N conversion efficiency (NCE). Experiments were established in 1994 and 1995 to evaluate impacts of six N fertilization levels (0–250 kg N ha–1) applied at the end of winter. Fertilization significantly increased forage dry matter (DM) and N accumulation in both years. A fitted critical NDC [Ncr (g kg–1) = 40.73DM (t ha–1)–0.379; r2 = 0.69] presented lower values than a published reference NDC. The NNIs calculated using the critical NDC showed higher values at higher N fertilization levels. The validity of the critical NDC and the usefulness of the NNIs should be tested in further experiments. High NUE values were observed in both years (44.20 and 52.21 kg DM kg–1 N applied in 1994 and 1995, respectively) although NUpE and NCE values varied between experiments.

Abbreviations: DM, dry matter • NCE, nitrogen conversion efficiency • Ncr, critical nitrogen concentration • NDC, nitrogen dilution curve • NNI, nitrogen nutrition index • Nopt, optimum nitrogen concentration • NUE, nitrogen use efficiency • NUpE, nitrogen uptake efficiency


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
THE MAINTENANCE of growth of good quality forage during winter is needed in temperate Argentinean grazing systems. Since low temperatures restrain growth of temperate forage grasses (Pollock et al., 1993), annual ryegrass, which is adapted to grow under low temperatures (Eagles et al., 1993), is commonly used as a winter forage crop. Although the growth response of forage grasses to low temperature is genetically regulated, it can be modified by other environmental factors such as nutrient availability (Collins et al., 1990; Chapman and Lemaire, 1993).

In spring, rates of DM accumulation are greater than in autumn or winter. This change in productivity coincides with the transition from vegetative to reproductive development and is associated with changes in several major physiological processes that alter the response of the grass crop to its environment (Parsons, 1988). Because N uptake and plant growth are interdependent processes (Touraine et al., 1994), a high N requirement during late winter and early spring has been observed for annual ryegrass (Salette et al., 1984). However, since the rate of soil N mineralization varies throughout the year, mainly in response to soil temperature and water status, N availability is one of the main factors limiting grass growth during winter and early spring in humid-temperate regions (Whitehead, 1995).

Different levels of nutrient content, from deficient to excessive or toxic, can be found in plants (Lawlor, 1991). Specifically, the critical level is the nutrient concentration in the plant below which a yield response to added nutrient occurs. Critical levels or ranges vary among crops and nutrients. At higher plant nutrient concentration, eventual yield increases will not be significant (Justes et al., 1994). Moreover, as plants can accumulate N and later remobilize it during the growth period (Millard, 1988), N concentration can increase beyond the critical value. From an agronomical point of view, this phenomenon is known as luxury consumption (Bloom et al., 1985).

Nutrient requirement is not constant during the plant vegetative growth cycle. Following defoliation, in early stages of regrowth, a high N supply is required to support leaf area development and photosynthesis. Thereafter, when the proportion of the low-N structural components in the forage increases (i.e., cell walls) (Caloin and Yu, 1984), N requirement per unit of incremental DM decreases (Greenwood et al., 1990).

Tissue N dilution during crop growth has been discussed by several authors (Lemaire and Salette, 1984; Caloin and Yu, 1984; Greenwood et al., 1991; Justes et al., 1994), and different mathematical models have been applied to describe it. Initially, Lemaire and Salette (1984) established the concept of the reference NDC. This curve describes the decline in the optimum N concentration (Nopt) as forage DM accumulates in temperate pastures according to the following equation:

[1]
where Nopt is the total N concentration in forage that produced the maximum amount of biomass, expressed as g N kg–1 forage DM; forage DM yield is expressed in t ha–1; 48 is a coefficient that represents the forage Nopt at 1 t DM ha–1; and 0.32 is a coefficient that characterizes the pattern of Nopt decrease during growth (Lemaire and Gastal, 1997). From this model, any actual N concentration below Nopt according to the reference NDC would limit crop growth. The model has been proposed as adequate to estimate N deficiencies during regrowth periods for different temperate grass swards, including different cultivated and natural species (Lemaire and Gastal, 1997).

Justes et al. (1994) proposed to apply a statistical procedure to determine a critical NDC in which the N concentration at each point of the NDC corresponds to the N concentration level (i.e., critical N concentration, Ncr) at which forage DM does not significantly increase despite an increased crop N uptake and forage N accumulation at higher N fertilization levels.

Many researchers have applied either the reference NDC (Greenwood et al., 1990; Bélanger et al., 1992; Bélanger and Richards, 1997) or the critical NDC (Justes et al., 1994; Colnenne et al., 1998) to predict the N nutritional status of different perennial temperate grasses. In this way, the NNI for a given accumulated forage DM can be estimated by the ratio between the actual forage N concentration and the corresponding Nopt calculated from the reference NDC or the Ncr calculated from the critical NDC, depending on the selected nonlimiting concentration. Such an index allows quantification of the intensity of the N deficiency (Lemaire and Meynard, 1997). However, there is not enough information on the application of these NDCs to estimate the N nutritional status of winter annual forage crops such as annual ryegrass.

In addition, losses of N into the environment have become a major concern. Consequently, NUE and its components, NUpE and NCE, have been studied (Ortiz-Monasterio et al., 1997; Dreccer et al., 2000). Differences among grass genotypes in NUE were found (Isfan, 1993; Wilkins et al., 1997), indicating that N requirements for achieving potential growth rates may also vary among genotypes. The knowledge of these coefficients in annual ryegrass is important to determine crop N requirements and to define N fertilization strategies that reduce N losses and, consequently, the risks of environmental contamination.

Our objectives were (i) to obtain a critical NDC for annual ryegrass winter–spring growth in the Humid Pampa of Argentina, (ii) to compare the obtained critical NDC with NDCs obtained previously by other authors for several temperate forage grasses, (iii) to estimate the NNI, and (iv) to determine NUE and its components NUpE and NCE.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Two experiments were conducted from March to October in the southeast of Buenos Aires Province, Argentina: one in 1994 in Tandil (37°14' S, 59°15' W) and the other in 1995 in Balcarce (37°45' S, 58°18' W). Soils for Tandil and Balcarce were fine, illitic, thermic Typic Argiudoll (Series Tandil) and fine-loamy, mixed, thermic Typic Argiudoll (Series Mar del Plata), respectively. In both cases, previous crops were mixed pastures. Average topsoil (0- to 20-cm depth) organic matter, NO–3–N, and P content (P Bray) were 55 and 57 g kg–1, 7 and 6.8 mg kg–1, and 18 and 13.3 mg kg–1, for Tandil and Balcarce, respectively. In both experiments, annual ryegrass cultivar Grasslands Tama was studied. Both crops were sown during the first week of March at 30 kg ha–1 of viable seed. Triple superphosphate was broadcasted and incorporated in the upper 10 cm of the soil at a rate of 50 kg P ha–1 before sowing. Climatic data are shown in Table 1. Accumulated temperature was determined from the sum of daily mean air temperatures (base temperature, 0°C) from the initial cut date until the end of the regrowth period.


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  		Table 1. Monthly mean temperatures for Tandil (1994) and Balcarce (1995), average monthly mean temperatures for 1970–1993 (Balcarce) and 1961–1990 (Tandil), monthly rainfall and average for 1970–1993 (Balcarce) and 1961–1990 (Tandil), and applied irrigation for 1995 (Balcarce). Source: Servicio Meteorológico Nacional, Fuerza Aérea Argentina (Tandil 1994) and Estación Agrometeorológica EEA INTA Balcarce (Balcarce 1995).

 
An initial cut to 2.5-cm height was conducted on 11 and 7 August in Tandil and Balcarce, respectively. In both experiments, N was surface-broadcasted as urea the following day at rates of 0, 50, 100, 150, 200, and 250 kg N ha–1 (named N0 to N250, respectively).

Forage yield was calculated for six successive dates (Tables 2 and 3) by harvesting independent plots of 5.5 m2 (2.5-cm cutting height) using a mower. A subsample of forage from each plot at each harvest was oven-dried at 60°C and ground. From a pooled sample of three blocks, total N concentration in plant tissue for each treatment at each date of harvest was determined by Method A (without salicylic acid modification) reported by Nelson and Sommers (1973).


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  		Table 2. Annual ryegrass winter–spring forage accumulation at different N fertilization rates in 1994.

 

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  		Table 3. Annual ryegrass winter–spring forage accumulation at different N fertilization rates in 1995.

 
Following each harvest, one quadrat (0.2 by 0.5 m) per plot was cut to ground level to estimate aboveground biomass below cutting height.

Apparent NUE was calculated as:

and it was partitioned into its components: NUpE and NCE. The first was estimated as:

while the second was calculated for the N fertilized treatments as:

To obtain the critical NDC, the procedure proposed by Justes et al. (1994) was performed. For this purpose, data of forage DM production under the different N levels were analyzed by ANOVA, and means were separated using Duncan's test. Then, minimum accumulated DM values not significantly different (P = 0.10) from the maximum forage DM accumulated for each harvest date were established as critical DM. Figure 1 illustrates a hypothetical variation of N concentration vs. forage DM for five possible N treatments at a given measurement date. The oblique line joins significant increases in forage DM and N concentration. The vertical line corresponds to increases in N concentration without significant changes in forage DM. The abscissa of the latter equals the mean abscissa of points N3 to N5. The Ncr corresponds to the ordinate of the intersection point of the oblique and vertical lines. Only forage yield values greater than 1 t DM ha–1 were considered because for lower values, the decrease in N concentration of aerial parts would not be significant since leaf self-shading and competition for light among plants are low (Justes et al., 1994). To compare our fitted critical NDC and the reference NDC (Lemaire and Salette, 1984), slopes and intercepts of linear regressions adjusted using the log-transformed values of forage yield and their corresponding log-transformed N concentration values were compared using dummy variables (Littell et al., 1991). Furthermore, NNI was calculated as the ratio between actual forage N concentration and Ncr values for each harvest date. Similarly, relative DM accumulation (relative DM) was obtained from the ratio between forage DM yield and critical DM for each harvest date.



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  		Fig. 1. Diagram representing tissue N concentration vs. accumulated forage dry matter (+). N1–N5 = values measured in different N fertilization treatments at a given date. • = calculated critical point at this date (adapted from Justes et al., 1994).

 
The experimental design was a split plot, with three randomized blocks in both years. Harvest dates were main plots, and N treatments were subplots. Critical NDC was obtained using the SAS NLIN procedure (SAS Inst., 1985). Linear (forage DM vs. N applied, N accumulation vs. N applied, and N uptake vs. N applied) and quadratic regressions (forage DM vs. N applied and forage DM vs. N uptake) were fitted using SAS (SAS Inst., 1985) GLM and REG procedures, respectively. The significance level used was 5% (P = 0.05) unless otherwise indicated. Slopes and intercepts of linear functions (N accumulation vs. N applied, relative DM vs. NNI, and NUpE) were compared using dummy variables (Littell et al., 1991). The models chosen to describe the forage DM accumulated in response to applied N were selected according to the highest coefficients of determination.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Forage and Nitrogen Accumulation during Winter–Spring Growth
As expected, N fertilization significantly increased forage yield in 1994 and 1995, but except in the fourth and fifth harvest dates of 1995, no further increases in forage yield were observed at N rates higher than 150 kg ha–1 (Tables 2 and 3). Similar responses were observed during winter–spring growth of oat (Avena sativa L.) (Marino et al., 1995), wheatgrass (Thinopyrum ponticum Podp.) (Fernández Grecco et al., 1996), winter forage crops (Mazzanti et al., 1997), and tall fescue (Festuca arundinacea Schreb.) (Lattanzi, 1998) in Balcarce.

Since differences in forage yield between years and the interaction of year x N rate were not significant, the overall response of total DM forage yield reached at the end of the experimental period to N applied in both years was found to be as shown in Fig. 2 . Forage yield for the control treatment (N0) represented 37 and 34% of N250 treatment in 1994 and 1995, respectively.



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  		Fig. 2. Annual ryegrass yield [forage dry matter (DM) accumulated, solid line] and forage N concentration (each observation corresponds to a pooled sample of three blocks, dashed line) for 1994 and 1995 in response to N fertilization at the end of the experimental period. Bars indicate standard errors of the means (SEM).

 
Increases in the level of N fertilization increased forage N accumulation in both years (Fig. 3) . During the first part of the growth periods, fertilized treatments showed an increase in N accumulation and reached the maximum values at the last harvest in 1994 (Fig. 3a). However, in 1995, the higher N treatments (N200 and N250) reached maximum N accumulation at the fourth harvest and decreased thereafter (Fig. 3b). This response has been observed previously (Imsande and Touraine, 1994). Similarly, Whitehead (1995) reported that in nondefoliated perennial ryegrass fertilized with 138 kg N ha–1, total forage N peaked a few days before flowering stems emerged and well before herbage yield was maximum.



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  		Fig. 3. Annual ryegrass N accumulation in forage for each N fertilization rate during winter–spring growth in (a) 1994 and (b) 1995. Bars indicate standard errors of means for sampling dates.

 
Nitrogen Concentration in Forage
Nitrogen fertilization increased forage N concentration in both years (Fig. 2 and 4) . Thus, on average for the experimental period, the lowest N concentration was observed in N0 (16.7 g kg–1 in 1994 and 12.5 g kg–1 in 1995) and the highest in N250 (37.9 and 33.9 g kg–1 in 1994 and 1995, respectively). These values are in agreement with previous results for forage grasses (Wilkins and Lovatt, 1989).



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  		Fig. 4. Annual ryegrass forage N concentration in relation to forage yield for each harvest date of 1994 and 1995, reference N dilution curve (Nref), critical N dilution curve (Ncr), and minimal (Nmin) and maximum (Nmax) forage N concentration. SE = standard error estimated from the Ncr regression.

 
As expected, forage N concentration decreased with time (Lemaire and Salette, 1984; Greenwood et al., 1990) in both experiments as shown in Fig. 4. Since nonsignificant differences were found among the critical NDC fitted for each data set considered (1994 and 1995), both data sets were pooled, and the following critical NDC was obtained (Fig. 4):

[2]

However, forage N concentration showed a large variability at a given level of forage DM accumulated. To illustrate this variation, two curves using maximum (Nmax) and minimum (Nmin) N concentration values in forage were fitted (Fig. 4):

[3]

[4]

Similarly, in oilseed rape (Brassica napus L.), Colnenne et al. (1998) found that Nmin = 20.7DM–0.17 and Nmax = 61.8DM–0.21.

The reference NDC adequately described the evolution of N concentration of the highest forage yields, which were obtained at the highest N rates, independently of soil and weather conditions (Fig. 4). These data are in agreement with previous papers (Lemaire and Salette, 1984; Bélanger et al., 1992; Bélanger and Richards, 1997; Lemaire and Meynard, 1997).

Interestingly, Ncr values were consistently lower (on average around 20% throughout the growth period) than those calculated by the reference NDC (Fig. 4) or those calculated by Greenwood et al. (1990) for C3 plants (N concentration = 56.97DM–0.5) and by Justes et al. (1994) for wheat (Triticum aestivum L.) (N concentration = 53.5DM–0.442). Similarly, Colnenne et al. (1998), using Justes et al.'s procedure in oilseed rape, found differences between the critical NDC and previous models.

The observed discrepancies among NDCs above might be caused by differences among species, experimental periods, cutting height, and/or statistical methods applied to distinguish limiting from nonlimiting N fertilization levels to obtain the critical NDCs. Genotypic differences in N concentration could be explained by differences in leaf weight ratio (i.e., leaf DM/forage DM) (Colnenne et al., 1998; Brégard et al., 2000) since stems have lower N concentration than leaves because of their higher proportion of structural tissues.

Nitrogen Nutrition Index
Crop N nutrition status is considered adequate when NNI is 1, limiting when it is lower than 1, and in excess when it is higher than 1. The excess of N can be stored as pools of different chemical forms comprising simple inorganic (nitrate) and complex organic compounds in plant tissues (Millard, 1988; Heilmeier and Monson, 1994; Brégard et al., 2000).

In coincidence with previous findings for several species (Lemaire et al., 1996; Colnenne et al., 1998), the NNIs calculated for annual ryegrass showed relatively low variation within N treatments through the growth period and showed higher values at higher N fertilization levels (Fig. 5) . For example, NNIs were lower than 0.5 for N0 and N50, close to 1 at N100 and N150, and were higher than 1.5 at N200 and N250. By definition, the crop maximum growth rate is achieved when NNI values are greater than or equal to 1 (Lemaire and Gastal, 1997). This is illustrated in Fig. 2 where it is shown that while forage N concentration increased in response to higher rates of applied N, nonsignificant differences in forage yields were observed beyond N100. Nitrogen nutrition values (Fig. 5) remained close to 1 for N100 during 1994 and for N150 during 1995. In both years, N200 and N250 presented values of NNI higher than 1.2, indicating a supra-optimal N nutrition level.



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  		Fig. 5. Evolution of the N nutrition index (NNI) for each N fertilization level during winter–spring growth in (a) 1994 and (b) 1995.

 
In situations where soil N supply varies during growth, as occurred in this experiment, estimations of NNI could be done at each harvest date for each N fertilization treatment. The relationship between values of NNI < 1 (plants growing under suboptimal N levels) and the corresponding relative DM accumulation is shown in Fig. 6 . The regression line obtained was not significantly different from the y = x line, demonstrating a close positive relation between variables and the ability of NNI to represent the N deficiency level.



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  		Fig. 6. Relationship between N nutrition index (NNI) and relative accumulated DM (DMac/DMcr) for different N fertilization levels during annual ryegrass winter–spring growth in (a) 1994 and (b) 1995.

 
In summary, to be able to use NNIs as a tool to correct annual ryegrass N deficiencies in the region, the validity of the critical NDC and NNIs shown in the present paper should be tested in further experiments.

Nitrogen Utilization in Annual Ryegrass
Apparent NUE was not different between years and, as expected, decreased with increasing N fertilization rates (44.20 and 52.21 kg DM kg–1 N applied for N50 and 17.61 and 15.02 kg DM kg–1 N applied for N250, in 1994 and 1995, respectively). The figures calculated were similar to those reported previously for several temperate forage grasses receiving high N fertilization levels (Whitehead, 1995).

The response to N applied (kg N accumulated kg–1 N applied, calculated as the slope of the relation among N accumulated and N applied) was significantly higher in 1994 than in 1995:

[5]

[6]

Similar to findings of Van Keulen and Stol (1991), NUpE and NCE showed linear and nonlinear responses, respectively (Fig. 7) , but values varied between years.



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  		Fig. 7. (a) Nitrogen apparent uptake efficiency (NUpE) and (b) N apparent conversion efficiency (NCE) in 1994 (solid line) and 1995 (dotted line). Bars indicate standard errors of means (SEM).

 
Nitrogen uptake efficiency was higher for 1994 than for 1995 (Fig. 7a). Under field conditions, soil N availability shows high spatial and temporal heterogeneity that affects plants' N uptake. During the winter and early spring of 1995, in spite of the irrigation, scarce rainfalls and relatively high mean temperature (especially in September, Table 1) could have determined short periods of soil water deficiency and, consequently, a decreased N uptake of the applied fertilizer (Bloom et al., 1985). In contrast, the higher water availability during the experimental period of 1994 (Table 1) in relation to the same period of 1995 might have favored a greater N uptake from the fertilizer applied.

The uptake rate of a given element depends on its external concentration and on the plants absorption capacity (Lee, 1993). Several authors have found that the maximal nutrient absorption capacity of plants is higher than that required to obtain the maximum yield (Jarvis and Macduff, 1989; Jeuffroy and Meynard, 1997). Justes et al. (1994) observed that, for a certain amounts of aerial biomass, the N concentration could be up to 160% of the N concentration considered critical. Nutrients such as N can be accumulated (stored) in plants during periods of external abundance and consumed in subsequent growth when they are externally limited (Bloom et al., 1985).

Higher values of NCE were found in 1995 than in 1994 (Fig. 7b). This means that a higher amount of forage per unit of N uptake was produced in 1995. The amount of N uptake required to produce the maximum forage accumulation was estimated as 186 and 106 kg N ha–1 for 1994 and 1995, respectively.

According to the previous discussion, the lower NCE during 1994 in relation to 1995 reflects a luxury consumption. In other words, in 1994, plants acquired N in excess for its current growth.

Macduff et al. (1989) have shown the ability of two Lolium genotypes to sustain DM production and growth during periods of N shortage from the utilization of amino acids, arising from protein turnover in old tissues as well as from stored NO–3. Consequently, the decline in N concentration in forage DM determined that the efficiency of N utilization was significantly increased.

The Ncr values obtained from the critical NDC for annual ryegrass winter–spring growth, estimated under a unique N application at the beginning of the regrowth period, were on average 20% lower than those obtained from the reference NDC. These results indicate that specific critical NDC, and hence the corresponding NNI, must be obtained for the different agronomical situations in which they are meant to be applied.


   ACKNOWLEDGMENTS
 
This study was supported by the Instituto Nacional de Tecnología Agropecuaria (Plan 077) and Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata (Project 15/A075). The authors gratefully acknowledge Dr. Gilles Lemaire for his helpful comments and the Unité de Recherche de Écophysiologie des Plantes Fourragères–INRA, Lusignan, France, for supporting the senior author during her research leave. Also, Dr. Mónica Agnusdei (INTA Balcarce) is greatly acknowledged for critical reading of the manuscript and valuable suggestions.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 





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