RESEARCH
Critical Nitrogen Concentration Declines
with Soil Water Availability in Tall Fescue
Pedro M. Errecart,* Mónica G. Agnusdei, Fernando A. Lattanzi,
María A. Marino, and Germán D. Berone
ABSTRACT
The diagnosis of the N status of crops is based
on the concept of critical N concentration (Ncr),
which is the minimum N concentration in shoot
biomass (SB) required for maximizing growth.
A reference curve of Ncr decrease (Ref-Ncr)
with SB increase proposed for C3 species
(Ref-Ncr = 48 SB-0.32) was validated for several
crops growing without water deficiency in different sites and seasons; however, the validity of
Ref-Ncr is uncertain when water is limiting. The
objective was to assess whether water stress
affects Ncr. Five regrowths of a temperate-type
tall fescue [Lolium arundinaceum (Schreb.) Darbysh.] were followed during autumn, spring,
and summer in Balcarce, Argentina. Several N
rates were applied and SB accumulation and N
concentration were measured in each of four to
six sequential SB harvests performed at every
regrowth. SB, Ncr, available soil water, reference evapotranspiration (ET0), and real evapotranspiration (RET) were estimated. Ncr agreed
well with Ref-Ncr when soil water was nonlimiting, but it was consistently lower than Ref-Ncr
whenever crop RET was reduced (RET/ET0 < 1).
Indeed, crop average Ncr during an entire
regrowth scaled linearly with the average level
of water stress in the period: (Ncr/Ref-Ncr)avg =
0.83 (RET/ET0)avg + 0.22 (R2 = 0.90, p < 0.0001).
Hence, while Ref-Ncr remains appropriate for
assessing crop N status under adequate water
availability conditions, the N nutrition management of water stressed crops should be guided
by their actual Ncr.
P.M. Errecart, M.G. Agnusdei, and G.D. Berone, Instituto Nacional
de Tecnología Agropecuaria (INTA), Estación Experimental
Agropecuaria Balcarce, Ruta 226 km 73.5, Balcarce, Argentina; F.A.
Lattanzi, Lehrstuhl für Grünlandlehre, Technische Univ. München,
D-85350, Freising-Weihenstephan, Germany; M.A. Marino, Facultad
de Ciencias Agrarias, Univ. Nacional de Mar del Plata, Ruta 226 km
73.5, Balcarce, Argentina. This publication is a partial requirement for
earning a PhD degree at the Univ. Nacional de Mar del Plata by P.M.
Errecart. Received 21 Aug. 2013. *Corresponding author (errecart.
pedro@inta.gob.ar).
Abbreviations: D13C, carbon isotope discrimination; DM, dry matter;
ET0, reference evapotranspiration; FTSW, fraction transpirable soil
water; Ncr, critical N concentration; NNI, N Nutrition Index; Ref-Ncr,
critical N concentration of reference; RET, real evapotranspiration; SB,
shoot biomass; SBcr, critical SB; SD, standard deviation.
A
n accurate diagnosis of the N status of crops is required
for the optimization of the N management at farm level.
This issue has permanent interest due to the environmental consequences of excessive N dressings and the high relative cost of
fertilizer N. An efficient N management should avoid the occurrence of episodes of excess N, aiming to match as best as possible
N availability (soil plus fertilizer) with crop N demand. Further,
in the case of perennial forage crops, N also influences sward persistence (Mackay et al., 2001) and species composition (Schwinning and Parsons, 1996).
Crop N demand at any time of crop growth cycle is the result
of crop growth rate and its Ncr (Lemaire and Gastal, 2009), Ncr
being the minimum N concentration in SB allowing to achieve
maximal instantaneous growth rates (Greenwood et al., 1990).
Published in Crop Sci. 54:318–330 (2014).
doi: 10.2135/cropsci2013.08.0561
© Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA
All rights reserved. No part of this periodical may be reproduced or transmitted in any
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318
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crop science, vol. 54, january– february 2014
Empirical observations of the decline of Ncr with SB
increase performed in several species (Lemaire and Salette,
1984; Greenwood et al., 1986, 1991) led to the formulation
of reference curves of Ncr dilution (Ref-Ncr) of the type:
Ref-Ncr = a SB -b
where a and b are coefficients physiological group-specific.
Such functions were suggested to be applicable at any growth
stage and to not vary substantially with major environmental factors (Gastal and Lemaire, 2002). Reference curves of
critical N concentration have been validated under different
pedoclimatic conditions (Justes et al.,1994; Colnenne et al.,
1998; Herrmann and Taube, 2004; Ziadi et al., 2008; Agnusdei et al., 2010), although in some cases, Ncr dilution curves
have shown to be species-specific (Justes et al., 1994; Colnenne et al., 1998; Marino et al., 2004), to be higher in the
seeding year of perennial forage crops (Bélanger and Richards, 2000), to be cultivar-specific (Bélanger et al., 2001), or
to decline steadily as perennial forage crops age (Bélanger
and Ziadi, 2008). The Ref-Ncr criterion then gave rise to the
method of reference for the assessment of crops N nutrition:
the N Nutrition Index (NNI), which is computed as:
NNI = crop current SB N concentration/Ref-Ncr
Crop yield is closely related to the NNI (Lemaire and
Gastal, 1997; Ziadi et al., 2008; Agnusdei et al., 2010),
which confirms the robustness of the concept of Ncr and
endorses the NNI as an efficacious tool for the analysis and
interpretation of agronomical data (Lemaire et al., 1995;
Lemaire and Meynard, 1997; Gonzalez-Dugo et al., 2005).
To be applicable, N nutrition diagnosis techniques
should ideally comply with at least two fundamentals:
(i) expeditiousness, and (ii) applicability under any circumstance. Concerning the first, Errecart et al. (2012)
reported a satisfactory field performance of two NNI
proxies of rapid measurement. Regarding the applicability of the NNI, a yet unclear point is whether the Ncr is
indeed constant under any environmental condition. An
eventual lower Ncr would lead to underestimations of crop
N status and excessive fertilizer N loadings.
Discrepancies between Ref-Ncr and actual Ncr have
indeed been observed in several studies. In wheat, shortened growth season and reduced soil water availability
have both been suggested as putative causes of the variability in Ncr among sites ( Justes et al., 1994; Ziadi et al.,
2010). In potato, a lowered Ncr was observed under water
stress (Bélanger et al., 2001). In forage crops, a lowered
Ncr has been observed under nonoptimal growth conditions by Agnusdei et al. (2010), who suggested water stress
and low temperatures as likely causes of the drop in Ncr.
The occurrence of restrictions to plant growth is the
rule rather than the exception in most areas of crop and
crop science, vol. 54, january– february 2014 forage production. Water stress episodes in particular are
highly recurrent, not only in the warm season, but also in
spring and autumn. However, we know of no study analyzing the relationship between Ncr and water stress. The
aim of the present study was, hence, to assess whether the
Ncr of a C3 forage crop is affected by water stress and, if
so, to test whether the magnitude of the change in Ncr is
related to the intensity of water stress.
MATERIALS AND METHODS
Experimental Site, Soils, and Climate
Experiments were performed at the Estacion Experimental Agropecuaria Balcarce (Instituto Nacional de Tecnología
Agropecuaria), Balcarce, Buenos Aires, Argentina (37°45¢ S and
58°18¢ W, 130 m asl). The climate is temperate subhumid-humid.
Monthly mean temperature ranges from 7.8°C in July to 21.4°C
in January. Average annual rainfall and ET0 are 990 and 950 mm,
respectively. Despite the high rainfall, water stress episodes are
common in the warm season, and also in spring and autumn.
Five regrowths were followed in a 9-yr old sward of a temperate type tall fescue [Lolium arundinaceum (Schreb.) Darbysh., formerly Festuca arundinacea (Schreb.)], ‘El Palenque MAG INTA’. Soil
tests were performed at the start of experiments. Four out of five
regrowths were carried out on a loamy textured Natraquoll (Soil
Survey Staff, 2010). Plant available water holding capacity up to
1 m depth was 56 mm, measured with the Richards membrane
pressure method (Dane et al., 2002). The 20 cm depth topsoil had
an organic matter content of 38 g kg-1, pH 9 (soil: water 1:2.5), P
content of 7 mg kg-1 (Bray I), an electric conductivity of 1.0 dS
m-1, and 19% exchangeable sodium. The regrowth followed in
early spring 2009 was performed on a loamy textured Argiaquoll
located nearby within the same paddock, with 59 mm plant available water holding capacity up to 1 m depth and topsoil organic
matter content of 96 g kg-1, pH 7.2, P content 8 mg kg-1, an
electric conductivity 0.1 dS m-1, and 11.3% exchangeable sodium.
Water Balance
Soil water balances were performed for each regrowth according to Della Maggiora et al. (2003), taking into account measured rainfall, irrigation, ET0, and soil plant available water. Soil
plant available water was constrained to a 1 m depth because
living roots were uncommon in deeper soil (data not shown).
Soil water balance computations started in 1 Aug. 2008 assuming a soil at field capacity, a soil condition assured by 112 mm of
rain over the previous 2 mo. ET0 was calculated after Allen et
al. (1998) from data recorded at the experimental site (iMETOS
ag weather monitoring station, Pessl Instruments GmbH, Weiz,
Austria). ET0 was assumed not to be affected by crop N status
(Caviglia and Sadras, 2001; Neves Lopes et al., 2011). Runoff was
assumed to be zero. RET was assumed equivalent to ET0 whenever the fraction of transpirable soil water (FTSW) was above 0.4
(Weisz et al., 1994; Allen et al., 1998; Ray and Sinclair, 1998).
For FTSW below 0.4, RET was assumed to decrease linearly,
yielding nil RET values at zero FTSW. Then, the daily RET/
ET0 ratio was estimated, which was considered as an instantaneous water stress index, theoretically ranging from 1 (RET =
ET0, no water stress) to 0 (nil RET, most severe stress possible).
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Table 1. Description of applied treatments and climatic conditions registered at each regrowth.
Regrowth
(fertilization date)
Early spring 2008 (21 Aug. 2008)
Late spring 2008 (23 Oct. 2008)
Autumn 2009 (19 March 2009)
Early spring 2009 (19 Aug. 2009)
Summer 2010 (30 Dec. 2009)
†
Real evapotranspiration.
‡
Reference evapotranspiration.
§
CAN, calcium ammonium nitrate.
N fertilization rates
and source
Mean incoming
global radiation
kg ha-1
0–75–150–225 Urea
0–75–150–225 Urea
0–75–150–225 Urea
0–75–150–350–500 CAN§
0–75–150–350–500 CAN
MJ m-2 d-1
14.4
22.2
12.1
As crop carbon isotope discrimination (D13C, in ‰) usually
decreases under water stress (Farquhar et al., 1989) and correlates
closely with plant available soil water in grasslands (Schnyder et
al., 2006), the accuracy of the RET/ET0 ratio as an estimator of
water stress was assessed by D13C measurements made as follows.
SB carbon isotope composition (d13C, in ‰), calculated as:
d C = ( C/ Csample)/( C/ CV-PDB standard)– 1
13
13
12
13
12
was determined in 0.7 mg of SB collected at the last harvest date
of regrowths with an elemental analyzer (NA1500, Carlo Erba
Strumentazione, Milan, Italy) interfaced to a continuous-flow
isotope ratio mass spectrometer (Deltaplus, Thermo-Finnigan
MAT, Bremen, Germany). Samples were measured against a
working gas standard previously calibrated against a secondary isotope standard (IAEA-CH6, accuracy ± 0.06‰ standard
deviation [SD]). A laboratory standard (wheat flour) was run
after every 10th sample to estimate the precision of the isotope
analyses ( ± 0.09‰ SD). The D13C was then estimated as:
D13C = (d 13Catm–d 13Csample)/(1000+d 13Csample)×1000
where d 13Catm is the 13C content of atmospheric CO2 (assumed
-8.3 ‰).
Sampling and Measurements
SB and N Concentration
In each subplot, a 0.1 m 2 (0.2 ´ 0.5m) quadrat was randomly
selected. Crop SB inside the quadrat was cut at ground level
with battery-powered shears. Senescent material was discarded.
Thereafter, samples were lyophilized (Rificor LA-B4, Rificor
SH, Buenos Aires, Argentina) and weighed to estimate accumulated SB (Mg ha-1). Samples were subsequently ground to
pass a 40-mesh screen in a Thomas Wiley Mini-Mill (Thomas
Scientific, Swedesboro, NJ, USA) and analyzed for total N concentration (g N kg-1 dry matter [DM]) according to Nelson
and Sommers (1973; Method A, without salicylic acid modification). Total N uptake in shoots (kg N ha-1) was estimated
as the product of accumulated SB ´ SB total N concentration.
Ncr, Ref-Ncr, and NNI
Crop Ncr (g N kg-1 DM) was estimated at each harvest date of
every regrowth. Harvest dates were not used for Ncr estimation if
SB did not differ among N treatments (p > 0.10). At each harvest
date, N rates whose SB accumulation did not differ (p > 0.10)
320
Mean air
temperature
13.1
21.5
(RET†/ET0‡)avg ratio
°C
9.4
15.1
13.3
0.71
0.51
0.63
9.3
20.7
0.85
0.71
from the maximum SB registered were defined as N-nonlimited.
The average SB of all N-nonlimited treatments was considered as
the critical SB (SBcr). Then, a linear function of the form:
N = a + b SB
was fitted to all replicates of N-limited treatments, and Ncr was
estimated as the N concentration at SBcr.
The Ref-Ncr (g N kg-1 DM) was calculated according to
Lemaire and Salette (1984) as:
Ref-Ncr = 48 SBcr-0.32
for SBcr values above 1.55 Mg ha-1. When SBcr was lower than
1.55 Mg ha-1, Ref-Ncr was assumed constant at 41.7 g N kg-1
DM ( Justes et al., 1994):
Ref-Ncr = 48(1.55)-0.32.
The NNI was estimated as the ratio of crop current N concentration to Ncr. A time-weighted average NNI (NNIavg) was
computed for each treatment with all the NNI values estimated
during regrowth, as proposed by Lemaire and Gastal (1997).
N nutrition index values above 1.0 were assumed as 1.0 when
NNIavg was regressed against treatment relative SB accumulation
(the ratio of treatment maximal SB accumulation to the maximal
SB accumulation observed in the regrowth), since improvements
in N status above the optimal condition would not affect plant
growth and would underestimate the detrimental effect on SB
accumulation of a period of N deficiency during regrowth.
Experimental Design and Treatments
Swards were cut at 5 cm height at the beginning of each regrowth.
Subsequently, a P amendment was surface broadcasted as calcium
triple superphosphate at a rate of 20 kg P ha-1 to provide nonlimiting P availability. Thereupon, treatments (four to five N rates
according to the regrowth, Table 1) were applied either as urea
or calcium ammonium nitrate. Immediately after fertilization, an
irrigation of 30 mm was applied to facilitate fertilizer N incorporation and minimize N losses through volatilization.
Treatments were arranged in a split plot design, replicated
in two blocks. N fertilizer levels were randomly applied to
the main plots. Main plots (18 m 2) were divided into subplots
which were randomly assigned to harvest dates. Four to six
forage harvests, depending on the regrowth, were performed
every 7 to 10 d (Supplemental Table S1).
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crop science, vol. 54, january– february 2014
Figure 1. Evolution of the FTSW (solid lines) and the RET/ET0 ratio (dotted lines) for five tall fescue regrowths. Vertical bars indicate dates
of shoot biomass harvest (FTSW, fraction transpirable soil water; RET, real evapotranspiration; ET0, reference evapotranspiration).
The effect of water stress on crop Ncr was evaluated in rainfed
regrowths. An identical set of regrowths was conducted in parallel following the same experimental design but under nonlimiting
water availability, provided by drip-irrigation (driplines spaced 0.60
m apart bearing 1 L hr-1 emitters every 0.30 m). Data from these irrigated regrowths, published in Errecart et al. (2012), was considered
here to: (i) verify the validity of the RET/ET0 ratio as an estimator
of water stress, (ii) evaluate the effect of soil water availability on crop
N uptake, and (iii) confirm the reliability of the method of estimation of crop Ncr.
Early spring 2008
Late spring 2008
Autumn 2009
Early spring 2009
Summer 2010
Statistical Analysis
RESULTS
Treatment means comparison (least significant difference test,
10% significance level) and ordinary least squares linear regression analysis were performed with the analysis of variance
(ANOVA) and REG procedures of the SAS package (v 9.0, SAS
Institute, Cary, NC, USA), respectively. Slopes and intercepts
of the linear functions were compared using dummy variables
(Littell et al., 2002). Nonlinearity was tested by assessing the
significance of an additional quadratic term.
Climatic Conditions and Soil
Water Availability
Data Digitization
Published data (Lemaire and Denoix, 1987a; Bélanger et al.,
1992; Justes et al., 1994; Bélanger and Richards, 2000; Plénet and
Lemaire, 2000; and Ziadi et al., 2008) were digitized using the
Engauge Digitizing software (http://digitizer.sourceforge.net).
crop science, vol. 54, january– february 2014 Table 2. Tall fescue carbon isotope discrimination (D13C)
measured at the last forage harvest of each regrowth, under
rainfed and nonlimiting water availability conditions.
Rainfed
Irrigated
————————— ‰ —————————
20.13
20.56
18.82
20.62
20.22
21.76
20.30
20.75
19.60
20.66
Experiments were run under a wide range of climatic
conditions. Mean incoming global radiation during the
experimental periods ranged from 12 to 22 MJ m-2 d-1,
and mean air temperature from 9 to 21°C (Table 1).
Likewise, rainfed regrowths developed under a wide
range of soil water availability. The estimated FTSW was in
general above 0.20 during most part of regrowths, but reached
a minimum of 0.03 in November 2008, when the estimated
RET/ET0 ratio also reached its lowest of 0.06 (Fig. 1). The
average RET/ET0 ratio for entire regrowths ranged from 0.51
(late spring 2008) to 0.85 (early spring 2009) (Table 1). Shortterm changes in the level of water stress within regrowths were
also substantial, as the estimated RET/ET0 ratio varied markedly even between consecutive harvest dates (Fig. 1).
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Support for the accuracy of the RET/ET0 ratio as an estimator of water stress is lent by D13C values. Under water stress
D13C was always lower (Table 2), and the estimated average
RET/ET0 ratio for each regrowth correlated well with the
ratio of D13C of rainfed to irrigated crops (Fig. 2). Thus, the
relative magnitude of water stress in rainfed plots was proportional to the magnitude of change in D13C, measured as the
deviation from D13C values observed in irrigated plots.
Sward Growth and N Uptake
Figure 2. Relationship between the average RET/ET0 ratio during
each of five tall fescue regrowths and the ratio of carbon isotope
discrimination in rainfed to irrigated plots at the last harvest date
(RET, real evapotranspiration; ET0, reference evapotranspiration).
N fertilization significantly increased both sward SB
accumulation and N uptake (Fig. 3). Under irrigated conditions fertilization increased SB up to 3.82 Mg ha-1 and
N uptake up to 140 kg ha-1 (both during summer 2010
regrowth), whereas under rainfed conditions these figures
Figure 3. N uptake in shoots vs. shoot biomass (SB) accumulation for five tall fescue regrowths grown either under irrigation (open symbols and dotted lines) or under rainfed conditions (solid symbols and solid lines). Colors represent different N rates (red: 0N; blue: 75N;
black: 150N; orange: 225N; purple: 350N; green: 500N).
322
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crop science, vol. 54, january– february 2014
Figure 4. Relationship between Ref-Ncr and estimated Ncr under rainfed conditions, when soil water balance indicated either
non-limiting water availability (solid squares) or water stress (open
squares). Solid triangles are Ncr datapoints estimated in two tall
fescue regrowths grown under irrigation (Ref-Ncr, critical N concentration of reference; Ncr, critical N concentration).
where 2.58 Mg ha-1 and 125 kg ha-1, respectively (both
during early spring 2009). Importantly, N uptake did not
differ significantly between rainfed and irrigated conditions at equivalent values of SB. This indicates that N
availability in rainfed plots was not affected by water stress
to the point of restricting N uptake.
Crop Ncr Dependence on the Level
of Water Stress
In irrigated plots, Ncr estimates agreed well with the
Ref-Ncr. Indeed, eleven Ncr values estimated over a wide
range of SB (1.09–6.30 Mg ha-1) averaged 97% of Ref-Ncr
(Supplemental Table S1, Fig. 4). This further verifies the
validity of the Ref-Ncr under nonlimiting conditions (see
also Errecart et al., 2012) and corroborates the reliability
of the Ncr estimation method used in the present study.
In rainfed conditions, Ncr estimates were also obtained
for an ample range of SB, both under conditions of nonlimiting water availability (i.e., RET/ET0 = 1; 1.50–4.02
Mg ha-1) and under reduced RET (0.90–4.57 Mg ha-1,
Supplemental Table S1). Whenever water was nonlimiting, estimated Ncr agreed well with Ref-Ncr. But under
conditions of reduced RET, Ncr was lower than Ref-Ncr
(Fig. 4). Further, estimated Ncr values expressed in relative
terms, as the ratio of Ncr to Ref-Ncr, correlated closely
with water stress. The Ncr/Ref-Ncr ratio associated significantly with several estimations of RET/ET0 made
at different time intervals before Ncr estimation (Fig. 5).
Even though the period of time before the Ncr estimation
in which soil water availability better predicted variations
in crop Ncr changed to some extent among regrowths,
the average level of water stress during the previous 11 d
always explained most variation in crop current Ncr and
was the best predictor when all regrowths were considered
simultaneously (R 2 = 0.65, Fig. 6). This indicates that the
interaction between crop Ncr and soil water was relatively
rapid. Over complete regrowths, the relationship between
both variables was also linear and very close. In fact, the
relative decrease in crop time-weighted average Ncr was
almost entirely accounted for by water stress (Fig. 7).
Figure 5. Percentage of Ncr/Ref-Ncr ratio variance explained by the RET/ET0 ratio estimated either the same day, several days before, or
averaged during different periods of time immediately preceding the date of Ncr estimation (Ncr, critical N concentration; Ref-Ncr, critical
N concentration of reference; RET, real evapotranspiration; ET0, reference evapotranspiration).
crop science, vol. 54, january– february 2014 www.crops.org323
Table 3. Effect of soil water availability on critical N concentration (Ncr) and sward N status estimation.
Ncr
RET
Regrowth N rate decrease† decrease§
Figure 6. Relationship between the average RET/ET0 ratio estimated during the period of eleven days previous to each harvest date,
and the estimated decrease in sward Ncr (RET, real evapotranspiration; ET0, reference evapotranspiration; Ncr, critical N concentration; Ref-Ncr, reference N concentration).
kg ha-1
0
Early Spring
2008
75
150
225
0
Late Spring
2008
75
150
225
0
Autumn
2009
75
150
225
0
Early Spring
2009
75
150
350
500
0
Summer
2010
75
150
350
500
N Status Under Water Deficit
Nitrogen fertilization significantly improved sward NNI
(Table 3). Nonlimiting N status was achieved in all regrowths,
except early spring 2008. Since Ncr decreased linearly with
increasing water stress (Fig. 6 and 7), assessing sward NNI after
the Ref-Ncr underestimated actual N status increasingly more
so as water stress intensified. In the most extreme case, RET
decreased by 49%, causing a decrease in sward average Ncr of
31% and a corresponding 30% underestimation of sward NNI.
Relationship Between N Status
and Forage Yield
Yields were directly related to crop NNI. When the effect
of soil water availability on crop Ncr was accounted for,
maximal SB accumulations were achieved with close to
nonlimiting N nutrition status (Fig. 8a). When NNIavg was
calculated after the Ref-Ncr (instead of the actual Ncr), the
relationship became biased, as maximal SB accumulations
were achieved at NNIavg substantially lower than 1 (Fig. 8b).
324
49.0
31.3
37.0
30.0
15.0
4.3
29.0
21.0
Ncr
Ref-Ncr
0.44
0.51
0.69
0.79
0.55
0.82
0.87
0.97
0.66
0.75
0.90
0.98
0.55
0.62
0.86
1.09
1.20
0.50
0.79
0.95
1.08
1.11
0.32
0.37
0.51
0.59
0.38
0.57
0.60
0.68
0.54
0.61
0.73
0.79
0.50
0.56
0.78
0.99
1.09
0.39
0.61
0.74
0.84
0.87
†
Real evapotranspiration decrease: [(1– RET/Reference evapotranspiration)*100].
‡
Computed up to 21 Oct. 2008 (later harvests were not considered in the analysis
because all N treatments differed in SB accumulation, hence there was no certainty
that the maximal N rate applied did not restrict crop growth).
§
Time-weighted average percentual decrease in critical N concentration = {1–[(Ncr/
Reference N concentration)avg]*100}.
¶
Figure 7. Effect of the average soil water availability condition during
regrowth on sward time-weighted average Ncr/Ref-Ncr ratio (RET,
real evapotranspiration; ET0, reference evapotranspiration; Ncr, critical N concentration; Ref-Ncr, critical N concentration of reference).
————— % —————
11.3
19.4‡
NNIavg¶ calculated
after the
Time-weighted average N Nutrition Index.
DISCUSSION
Nitrogen availability and water stress are the two major
limitations to crop production (Sinclair and Rufty, 2012).
In assessing whether soil water availability levels limiting
crop RET affect crop Ncr, the present work confirms the
validity of the Ref-Ncr under nonlimiting water conditions, and demonstrates that crop Ncr is systematically
lower than the Ref-Ncr under water stress, providing a
quantitative analysis of such effect on different seasons on
tall fescue, a forage crop.
Notably, the magnitude of the deviation of Ncr from
the Ref-Ncr scaled linearly with water stress intensity
as measured by the RET/ET0 ratio (Fig. 6 and 7). This
means that there is no unique Ncr dilution curve valid for
all water stress conditions, and we must instead think of a
family of Ncr dilution curves. Ncr continuously responds
to the prevailing RET/ET0 conditions, and the time of
this adjustment seems to be 11 d, on average (Fig. 6).
Cross-validation of the Relationship
Between RET/ET0 and Ncr/Ref-Ncr
Agnusdei et al. (2010) reported Ncr dilution curves significantly lower than the Ref-Ncr dilution curve in four
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crop science, vol. 54, january– february 2014
Figure 8. Relationship between treatment relative shoot biomass (SB) accumulation and its time-weighted average N nutrition index
(NNIavg) calculated after a) taking into account the effect of soil water availability on the critical N concentration, or b) the critical N concentration of reference (Ref-Ncr). Maximal SB is the highest SB accumulation achieved among the N rates applied at each regrowth. Data
from early spring 2008 regrowth was not included, since non-limiting N nutrition status was not achieved.
regrowths of C3 forage crops in which growth conditions
were not optimal. Soil water balances for each of these
regrowths were computed to estimate the daily RET/
ET0 ratios and calculate the corresponding Ncr using the
relationship presented in Fig. 6. The relationship between
observed Ncr values (Agnusdei et al., 2010, their Fig. 6a)
and our Ncr estimations is presented in Supplemental
Fig. S1. The estimated Ncr values compared very well to
observed ones for AR94, which was the only regrowth
out of the four characterized by low rainfall, resulting in
an average RET/ET0 ratio of 0.75. In contrast, predicted
and observed NNIavg values disagreed for the other three
regrowths, in which growth conditions were suspected as
not optimal due to factors other than water stress, like low
temperatures. This independent validation of the relationship between Ncr and RET in an annual species suggests
that the relationship reported in Fig. 6 may be robust.
Can Crop Ncr be Appropriately Estimated
Under Water Stress Conditions?
One issue regarding the estimation of Ncr that arises when
crop growth rates are low is that the statistical approach
may be biased. This is because the lower responses of SB
to N fertilizer when growth is limited, e.g., by water
stress, may be regarded as statistically nonsignificant, and
thus, both SBcr and crop Ncr would be underestimated.
In our study, however, this effect was not substantial as
estimated SBcr values were consistently close to maximal
SB accumulations.
A second issue is that soil N availability is often impaired
under water stress, mainly due to reductions in N mineralization and transpiration-related N fluxes to the roots (reviewed
by Gonzalez-Dugo et al., 2010). If N supply is limited to
the extent that it cannot meet crop N demand, Ncr would
be estimated under nonpotential N availability conditions,
and thus, would be underestimated. The consequence of
such N-supply limitation is a lowered N uptake at equivalent
crop science, vol. 54, january– february 2014 values of SB under water stress than under nonlimiting water
availability conditions (Lemaire and Denoix, 1987b; Lemaire
et al., 1996). In the environment of the present study, however, as Fig. 3 shows, crop N uptake followed fairly the same
pattern under both water availability conditions; that is, there
were no significant differences in crop N uptake between
rainfed and irrigated conditions at equivalent values of SB.
The difference in N uptake linked to soil water availability
can thus be entirely attributed to the effect of drought on SB
accumulation. Even under water stress conditions reducing
SB accumulation up to 2.7 Mg ha-1 in late spring 2008 (Fig.
3), tall fescue was able to absorb N at a rate high enough to
maintain its SB N concentration. These results suggest that
soil N relative availability was not altered by water stress; that
is, sward growth was reduced in a similar proportion as soil
N availability to the plant. Hence, N uptake should keep
increasing when SB has already reached its plateau. This is
indeed demonstrated in Fig. 9, which shows the simultaneous changes in crop SB and N uptake achieved with increases
of the N fertilization rate, for those treatments defined statistically–after their SB accumulation did not differ at p =
0.10– as non N-limited. As Fig. 9 shows, the changes in crop
N uptake registered in our work are well in agreement with
those calculated from several reports from the literature also
estimating crop Ncr (Lemaire and Denoix, 1987a; Bélanger
et al., 1992; Justes et al., 1994; Bélanger and Richards, 2000;
Plénet and Lemaire, 2000; and Ziadi et al., 2008). Finally, the
reliability of the Ncr estimations made under the growth limiting conditions prevailing in our study was further corroborated when sward growth showed to be much better related
to sward N status assessments performed after the actual Ncr
than after the Ref-Ncr (Fig. 8).
Why does Ncr Decrease Under Water Stress?
Previous water availability conditions defined sward relative Ncr (Fig. 6 and 7). Such a relationship between Ncr/
Ref-Ncr and RET/ET0 implies a fractional decrease in
www.crops.org325
Figure 9. Simultaneous changes in tall fescue shoot biomass (SB)
and N uptake achieved with increases in the N fertilization rate, for
N treatments defined statistically (based on their SB accumulation
not differing at p = 0.10) as non N-limited (X-axis: SBnon N-limited treatmentaverage SBall non N-limited treatments; Y-axis: N uptakeHigher N rate- N
uptakeLower N rate). Literature data was obtained from Bélanger et al.
(1992); Bélanger and Richards (2000); Justes et al. (1994); Lemaire
and Denoix (1987a); Plénet and Lemaire (2000); and Ziadi et al. (2008).
crop Ncr with water stress, and this type of decrease would
only be possible if drought would decrease just the ‘a’ coefficient of the Ncr dilution curve, without affecting the ‘b’
coefficient. Variations in the ‘b’ coefficient imply SB-associated changes in the Ncr/Ref-Ncr ratio; hence, if the ‘b’
coefficient were to change under water stress, the addition
of SBcr as regressor variable should improve the percentage of the Ncr/Ref-Ncr ratio variance explained by the
simple regression against RET/ET0. The R 2 of the multiple regression including SBcr was, as supposed, not significantly higher than that of the simple regression (0.654
vs. 0.646). Moreover, when the dataset was split into two
SBcr groupings (above and below 2.5 Mg ha-1, [Fig. 6])
and linear regressions were fitted, neither the slopes (p >
0.20) nor the intercepts (p > 0.15) of the regression of
Ncr/Ref-Ncr as a function of RET/ET0 differed between
groups. Thus, after Fig. 6 and for our growing conditions,
we propose the following Ncr dilution curve:
Ncr = a’ SB -0.32,
where
a’ = 20.6 + 28.3 RET/ET0 ratio.
One possible cause of the lowered Ncr under water stress is
increased concentration of water soluble carbohydrates leading to a passive decrease in shoot N concentration. This is a
plausible mechanism, as the concentration of water soluble
326
carbohydrates often increase in droughted plants (Karsten
and MacAdam, 2001; Shaimi et al., 2009), although it is
unclear whether this change is as linearly related to water
stress as the drop in Ncr. The Ncr dilution process has been
proposed to result from a compartmentation of plant SB in
“structural SB (SBs)” and “metabolic SB (SBm)” fractions,
having respectively low (Ns%) and high (Nm%) N concentrations (Lemaire and Gastal, 1997). Then, Ncr dilution
results from the ontogenetic decline of SBm/SB as plants get
larger. A third component of SB may thus be needed, SBr
(for reserves), that being mainly carbohydrates would have a
minimal Nr%. As water stress escalates, SBr should become
more important leading to a lowered Ncr.
Another hypothesis concerns differential responses
to water stress of allocation of dry mass vs. N. Water stress
increases allocation belowground (review Poorter et al., 2012).
If this change is greater for N than for dry mass, then shoot N
concentration would decrease. Again, the framework of Ncr
dilution would need to be extended to include roots.
A third possibility is that the lower growth rates under
water stress require less N for metabolic purposes. For
instance, photosynthetic rates are lower under water deficit conditions, and less N is needed in the photosynthetic
apparatus to reach maximal assimilation rates (Ghashghaie
and Saugier, 1989; Perniola et al., 1999; Shangguan et al.,
2000). A fourth hypothesis involves accelerated leaf senescence, and consequently increased N mobilization, under
water stress (Gan and Amasino, 1997). This would also
lower Nm%. The process of N mobilization is not included
in the theory of N dilution.
The first two putative mechanisms are congruent
with the observation that the magnitude of the decrease
in Ncr is independent of SB, i.e., water stress would affect
only the ‘a’ coefficient of the Ncr dilution curve. The
latter two are not. As both imply effects on Nm%, they
would modify the SBm/SB ontogenetic decline, and thus
their magnitude would depend on SB, i.e., would affect
the ‘b’ coefficient of the Ncr dilution curve. This was not
observed in the present study (Fig. 6 and 7). More research
is needed to clarify the causes of the Ncr decrease, particularly under field conditions.
Interpreting the Effect of a Lower Ncr
Under Water Stress in Terms of Crop
N Demand and its NNI
The balance between soil N supply and crop N demand
defines crop N status (Durand et al., 2010; Gonzalez-Dugo
et al., 2010). A lowered Ncr under water stress implies that
plant N demand for maximizing growth decreases relative
to that under not limited RET. Even when soil N supply
typically decreases under water stress (Garwood and Williams, 1967), we did not observe a limitation strong enough
to restrain N uptake; in general, N continued accumulating
in shoots whereas SB did not (Fig. 9). In fact, water stress
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crop science, vol. 54, january– february 2014
Figure 10. Evolution of the RET/ET0 ratio (solid rhombi) and the NNI for five N treatments during the Summer 2010 regrowth (circles: 0N;
triangles: 75N; inverted triangles: 150N; open rhombi: 350N; squares: 500N). Bars show registered rainfall (RET, real evapotranspiration;
ET0, reference evapotranspiration; NNI, N Nutrition Index).
did not induce N deficiency but rather improved crop N
status (Table 3), as it reduced crop N demand more than N
supply, because water stress decreased both SB accumulation and the amount of N required per unit of accumulated
SB. This is evident in the short-term dynamics of NNI.
For instance, in the summer 2010 regrowth, the NNI of
all treatments increased while soil water availability was
decreasing, up to 28 Jan. 2010 (Fig. 10). From that date
on, such upward trends in crop N status reverted when
rainfall events increased soil water availability; somewhat
later for the higher N rates, surely owing to a larger soil N
supply in those conditions. Hence, during the first part of
the regrowth period the soil supplied N in excess of a water
stress-reduced N demand. This is the first report in the bibliography describing such an increase in crop NNI under
water stress, in contrast with previous studies reporting
either no significant changes (Gonzalez-Dugo et al., 2005)
or decreases (Duru et al., 1997) in crop N status under such
conditions. If crop NNI would be recomputed after the
Ref-Ncr, an analysis of the evolution of crop N status during the Summer 2010 regrowth would indicate that–albeit
at a lower degree– crop NNI would still be increasing during water stress (data not shown). Hence, the discrepancy
between the referred works and our study must be ascribed
not only to a different estimation of crop N demand under
water stress–that is, estimating crop N status after the RefNcr or after the actual Ncr–but also to different levels of soil
N supply between droughted environments. Indeed, water
deficit seemed to not alter soil N relative availability in
the environment where our study was performed (Fig. 3).
Thus, soil N fluxes towards roots, which must have been
reduced under water deficit (Durand et al., 2010; Errecart
crop science, vol. 54, january– february 2014 et al., 2010), still provided N in excess for the decreased
N demand exerted by the sward under reduced soil water
availability conditions. The extensive root system of the
10 yr old tall fescue sward of our work could account, at
least partially, for the high capability of N capture of this
pasture, since root length density defines the diffusive N
flux, which is the component of soil N fluxes gaining relevance under water stress (Durand et al., 2010; Errecart et
al., 2010). Indeed, observed values of root length density
in the 0 to 10 cm soil horizon (35 cm root cm-3 soil) were
much higher than those reported by Gonzalez-Dugo et al.
(2005) for a tall fescue sward in the establishment year (6
cm root cm-3 soil). Traits like root dry weight and length
density, root hair development and viability, have all been
already reported to have major effects on tall fescue performance under drought (Huang and Fry, 1998; Huang,
2001; Sun et al., 2013).
Practical Implications
A consequence of a lower Ncr under water stress is that
in such situations, NNI assessments based on the Ref-Ncr
underestimate crop actual N status. This effect can be significant; crop NNI was underestimated up to 30% under
water stress (Table 3, Fig. 8). Further, assessing tall fescue
N status after the Ref-Ncr would have wrongly labeled
as N deficient several N-nonlimited treatments (see also
Agnusdei et al., 2010). This has important practical implications. For one, the amount of fertilizer N required to
reach a given N status changes. For instance, under a condition of water availability significantly restricting sward
RET and growth like summer 2010 regrowth, achieving
an NNI of 0.8 required approximately 100 kg of fertilizer
www.crops.org327
N ha-1. Had sward N assessment been performed after the
Ref-Ncr, 220 kg of fertilizer N would have been needed.
This analysis has the advantage of hindsight, but it is necessary to correct future fertilizer N dressings of crops
based on the reported effect of water availability on Ncr.
As Fig. 7 shows, knowing the average RET/ET0 ratio of a
future sward regrowth would allow fine-tuning fertilizer
N applications. Incorporating the concept of Ncr decrease
under water stress in crop models should help to achieve
such an objective. Several challenges could arise, and one
of them will be predicting the average RET/ET0 ratio of
future regrowths. For this, historical rainfall and ET0 data,
or the output of weather forecasting models could be used.
Here, we addressed the challenge of developing predicting functions for the Ncr/Ref-Ncr ratio, as we obtained
one for tall fescue and further validated it in annual ryegrass. Thus, it seems to hold for the edaphic environment
predominating in southeast Buenos Aires. However, the
threshold in FTSW at which crops start experiencing
stress can differ among species and even among environments (Allen et al., 1998), hence it would be necessary to
test whether similar relationships emerge with other crops
or under differing growing conditions.
CONCLUSIONS
This work demonstrates that when soil water availability
limits crop evapotranspiration, the Ncr is lower than under
nonstressed conditions. In tall fescue, Ncr increasingly and
linearly diverged from Ref-Ncr as the estimated RET/
ET0 ratio decreased. Therefore, the use of the Ref-Ncr
curves would underestimate the N status of water stressed
crops. An accurate estimation of NNI could be made
using Ncr values derived from functions relating the relative decrease in Ncr to the magnitude of water stress. In
the present study, the ratio of RET to ET0 showed promising value as an index of water stress that would allow to
adjust fertilizer N loadings after historical or forecasted
climatic data, to better meet crop N demands.
Supplemental Material Available
Supplemental Material includes Table S1 (measured SB
and N concentration, estimated Ncr and calculated RefNcr for each harvest date of five rainfed and two irrigated
tall fescue regrowths) and Fig. S1 (cross-validation of the
obtained RET/ET0 vs. Ncr/Ref-Ncr relationship with the
independent dataset of Agnusdei et al., 2010).
Supplemental Fig. S1. Relationship between the timeweighted average N nutrition index (NNIavg) reported by
Agnusdei et al. (2010) and the NNIavg calculated after computing soil water balances, estimating daily soil water availability and calculating the corresponding crop critical N
concentration (Ncr), for four regrowths of C3 forage crops:
tall wheatgrass 1999 (TW99), oats 1995 (O95), tall fescue El
Palenque 1996 (TF EP96), and annual ryegrass 1994 (AR94).
328
Acknowledgments
This study was financially and technically supported by the
Instituto Nacional de Tecnología Agropecuaria (INTA) Project
PE-AEFP 262921. F.A. Lattanzi received funding from DFG/
BMZ (LA2390/1-1). Authors wish to thank three anonymous
referees for their comments and also Dr. Gilles Bélanger, Dr.
Francois Gastal, and especially Dr. Jean-Louis Durand, and Dr.
Gilles Lemaire for the interest shown in this work and the valuable comments made.
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