Field Crops Research 58 (1998) 213±221

Nitrogen and water effects on wheat yield in a Mediterranean-type

climate. II. Fertilizer-use ef®ciency with labelled nitrogen
S. Garabeta,*, J. Ryana, M. Woodb
a
Natural Resource Management Program, International Center for Agricultural Research in the Dry Areas (ICARDA),
P.O. Box 5466, Aleppo, Syria
b
Department of Soil Science, University of Reading, P.O. Box 233, Reading, UK
Received 29 January 1997; received in revised form 27 March 1998; accepted 16 April 1998

Abstract

Under the Mediterranean farming conditions of Syria, rain-fed cropping predominates, but irrigation is increasing where water
sources are available. In both rain-fed or irrigated systems, it is important to understand N use by crops and its behavior in the
soil. In this paper, we report on nitrogen fertilizer-use ef®ciency (NFUE) by wheat (Triticum aestivum L.) under 1/3, 2/3 and
full irrigation with 15N-labeled fertilizer at different application rates (0, 50, 100 and 150 kg N haÿ1) for two seasons with
varying rainfall, i.e. 323 and 275 mm. NFUE values in the above-ground crop varied with measurement date, reaching a
maximum before anthesis, and then, during the grain-®lling period, either remaining constant under irrigation or decreasing,
particularly under the rain-fed conditions. Irrigation increased the recovery of applied N in grain and straw at harvest from
10% in the wetter year to over 60% in the drier year. Nitrogen at 100 kg haÿ1 level increased recovery by >45% in the wetter
year, while fertilizer recovery improved in the drier year only with enhanced water availability from irrigation. The Difference
method (28±95%) for estimating N recovery diverged from the 15N Direct method (21±63%), emphasizing the need to
examine both labeled, and unlabeled, N pools for interpretation of 15N studies. With irrigation, the crop removed signi®cantly
more fertilizer N than under rain-fed conditions, with less remaining in the soil; over 40% of the fertilizer N remained in the
top 20-cm soil as organic N. Irrigation had no effect on the 15N recovery at depth, with no signi®cant re-mineralization being
detected. While NFUE is increased by higher rainfall and irrigation, fertilizer N losses under the Mediterranean climatic
conditions of Syria are low. The apparent inef®ciency induced by organic immobilization adds to total soil N, which can
potentially be used by future crops. # 1998 Elsevier Science B.V. All rights reserved.
15
Keywords: Ammonium sulfate; N balance; N ®eld experiment; Net N mineralized

1. Introduction related (Harmsen, 1984), loss of nitrate from the

In the dry areas of West Asia and North Africa
(WANA), fertilizer N response is largely rainfall-
*Corresponding author. Tel.: +963 21 213 433; 312 477; fax:
+963 21 213 4900; 225 105; e-mail: s.garabet@cgnet.com
rooting zone through deep leaching is rare, but ammo-
nia volatilization may be a major N-loss mechanism
under certain conditions in such calcareous soils (Vlek
et al., 1981). However, Abdel Monem (1986) attrib-
uted the relatively low N loss (11±18%) from urea
fertilizer in clay soils in northwest Syria to the high

0378-4290/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved.

PII S0378-4290(98)00096-3
214 S. Garabet et al. / Field Crops Research 58 (1998) 213±221
cation-exchange capacity (CEC>50 cmol‡kgÿ1),
which promotes ammonia retention on exchange
sites.
Supplemental irrigation in the WANA region,
beginning in the spring with the onset of increased
evaporative demand and soil water de®cit, is designed
to increase and stabilize yield (Perrier and Salkini,
1991). The higher yields under supplemental irriga-
tion also promote fertilizer use. Nevertheless, the low
recoveries of applied N in rain-fed wheat (Abdel
Monem, 1986; Pilbeam et al., 1997) suggest the need
to improve N-use ef®ciency.
Under dry conditions, N ef®ciency at harvest gen-
erally ranges from 20 to 80%, depending on factors
such as fertilizer type (Abdel Monem, 1986; Pilbeam
et al., 1997), application time and method (Malhi and
Nyborg, 1992), soil type and climatic conditions
(Fillery and McInnes, 1992; Pilbeam, 1996). While
NFUE can be calculated by two methods: labelled
(Direct) and unlabelled (Difference) N fertilizer, it is
possible to distinguish between N derived from ferti-
lizer and from the soil pool only with the isotopic
tracer method (Hauck and Bremner, 1976). The Direct
method is based on 15N recovery by crops growing in
15
N-fertilized plots, while the Difference method is
calculated by the difference in plant N uptake in
fertilized and unfertilized plots. Estimates of NFUE
using 15N are usually lower than those calculated by
the Difference method (Harmsen and Moraghan,
1988; Palta and Fillery, 1993), while the extent of
such differences varies depending on crop and envir-
onmental conditions.
Most NFUE studies using 15N are presented as
balance sheets at crop maturity (Pilbeam et al.,
1997). While N uptake kinetics by plants during the
growing season under winter-rainfall Mediterranean
conditions have been investigated (Mary et al., 1987),
little attention was given to supplemental irrigation,
and considerable differences exist between the calcar-
eous clay soils in Syria (Abdel Monem, 1986) and the
sandy or duplex soils reported from Australia (Palta
and Fillery, 1993), where a Mediterranean climate also
occurs.
Thus, the aims of the 15N-fertilizer experiment
described here were as follows:
(a) to measure yield and the N accumulation by
rain-fed and irrigated wheat throughout the season;
(b) to assess the impact of irrigation on grain and
above-ground plant recovery of fertilizer N under
field conditions; and
(c) to construct a fertilizer N balance.
A secondary objective was to compare 15N isotope and
difference methods for determining NFUE. While
yield and N accumulation data for wheat grown under
Mediterranean climatic conditions of Syria were pre-
sented in the first paper (Garabet et al., 1998), this
companion paper describes NUE during the same two
seasons.
2. Material and methods
Full description of the site, climatic conditions
during the experimental period, N fertilizer rates
and irrigation treatments are found in Garabet et al.
(1998). Brie¯y, wheat was sown after a lentil crop in
1991/92 (mid-November) and a wheat crop in 1992/
93, with 3 weeks delay in the latter year (early
December). 15N-fertilizer (ammonium sulphate) was
applied on micro-plots (21 m2) in the main plots
(45 m2) at various rates (0, 50, 100 and 150 (kg
N) haÿ1). Supplemental irrigation was applied at 0,
1/3, 2/3 and full ®eld capacity to wheat from heading
onwards for two growing seasons, i.e. 1991/92
(323 mm) and 1992/93 (275 mm). Yield, N-uptake
and recovery of 15N in the above-ground crop was
monitored at 2-week intervals each year. Soil samples
were taken from micro-plots three times after sowing
(35, 140, and 216 days in Year 1, and 38, 120, 184 days
in Year 2) each season to monitor N dynamics in both
unfertilized and fertilized (100 (kg N) haÿ1), and rain-
fed and full irrigated, treatments for the four repli-
cates, which involved 16 plots. Nitrogen concentra-
tions were calculated on an area-basis by multiplying
%N by the bulk density (1.0±1.3 g cmÿ3) in the
respective layers.
Inorganic N was determined in soil samples in
150 ml 2M KCl (NH4±N) and of deionized water
(NO3±N) per 30 g fresh soil after shaking for 1 h
(Buresh et al., 1982). The 15NH4±N and 15NO3±N
forms in these extracts were separated with MgO, i.e.
Devarda's alloy. During distillation, cross-contamina-
tion was prevented by distilling ethanol between
samples and, subsequently, by passing steam through
 S. Garabet et al. / Field Crops Research 58 (1998) 213±221 215

the apparatus with the condenser-cooling water turned

off (Pruden et al., 1985). The ammonia gas evolved
was trapped in 0.01 N H2SO4 and the solution eva-
porated to dryness in glass vials. The 15N/14N ratio
analysis and total N (expressed on an oven-dry basis,
105EC) were determined by a CN-Roboprep mass
spectrometer.
15
2.1. Interpretation of total N and N data

Percent NFUE was calculated by two methods: 1)

Difference (N uptake in fertilized plotsÿN uptake in
control plots)/(applied N)100. 2) Direct (atom %
excess 15N in above-ground crop, corrected for 15N
recovered in plots receiving no 15N-labelled fertili-
zertotal N accumulation in fertilized plots)/(atom %
excess 15N fertilizerN application rate)100. Plant
N concentrations were comparable with those outside
the micro-plots, with <5% difference between them.
Therefore, we used N concentrations from micro-plots
in our calculations. After analysis of variance, least
signi®cant differences (LSD) were used to compare
treatment means.

3. Results

3.1. Seasonal assessment of nitrogen fertilizer-use

efficiency
Estimates of NFUE varied with the season, being
25% higher in the wetter Year 1 than in the drier Year 2
(Fig. 1). Compared with the Direct method, these
values were 14% higher by the Difference method
in Year 1 as compared to 26% higher in Year 2.
Maximum ef®ciency occurred well before harvest,
i.e. at heading (146 and 124 days after sowing in Year
1 and Year 2, respectively), after a period of rapid
growth from tillering to stem elongation. This was
followed by a signi®cant decrease in ef®ciency with
rain-fed and irrigated treatments in the wetter year
(Year 1); however, in the drier year NFUE decreased
only under rain-fed conditions. Differences due to
irrigation were signi®cant (Pˆ0.05) only in the drier
second year (1992/93). In both years, the effect of
irrigation was maximized by the ®rst irrigation
applied; the latter applications did not signi®cantly
affect N-use ef®ciency.
Fig. 1. Nitrogen fertilizer-use efficiency (100 kg haÿ1 rate) by the
Direct and Difference methods for wheat at different sampling
dates in two seasons. Error bars indicate least significant difference
(Pˆ0.05).
3.2. Final harvest
While irrigation and N application tended to
increase NFUE values obtained by the Direct method,
the trend with the Difference method was less obvious
in the wet year (Fig. 2). In that year, NFUE ranged
from 41 to 95% by the Difference method, compared
with 31 to 58% by the Direct method; corresponding
values were 28±60% and 21±63% in the drier year.
Additionally, NFUE varied more with the Difference
method (CVˆ24% for Year 1, and 30% for Year 2)
than with the Direct method (CVˆ11 and 17%,
respectively). In both years, overall means of NFUE
values (66% for Year 1 and 49% for Year 2) by the
216 S. Garabet et al. / Field Crops Research 58 (1998) 213±221
Fig. 2. Nitrogen fertilizer-use efficiency by the Difference and Direct methods for wheat in two seasons.
Difference method were higher compared with the
Direct method (45 and 39%, respectively). However,
the discrepancy between the two methods was smaller
in Year 2 (10%) than in Year 1 (20%).
As the variation was high with the Difference
method, we will concentrate on the results obtained
by the Direct method for subsequent interpretation of
NFUE. In Year 1, ef®ciency was increased with
increased N fertilizer rates, with a moderate increase
by irrigation; while in the second year, it was increased
by both N and irrigation levels with a signi®cant
(Pˆ0.05) interactions between them.
Irrigation had a moderate effect on NFUE in Year 1
and a marked effect in the drier Year 2; the greatest
increase was observed at the ®rst irrigation level (a),
particularly in Year 2, with NFUE increases of 41, 62,
and 88% for the three N levels, respectively; the
increases in Year 1 were only 0, 15 and 11% with
the same N application rates.
With the Direct method, NFUE substantially
increased with N fertilizer rates in Year 1, particularly
at 100 (kg N) haÿ1, but levelled off at the highest
(150 kg haÿ1) N rate. In Year 2, NFUE values sig-
ni®cantly (Pˆ0.05) increased as the N application rate
increased from 50 to 150 (kg N) haÿ1. Thus, both N
and water were major yield determinants in Year 2,
re¯ecting the low soil N content (<50 (kg N) haÿ1,
mainly in the 40-cm soil layer) and the limited water
available from rain alone.
3.3. Soil N recovery
Recovery of soil inorganic N at different sampling
times was inversely related to growth and uptake
(Table 1); at the season's end, only 20±30% of the
added N was recovered in the soil under rain-fed
conditions, while in irrigated plots, virtually none
remained in the soil following the addition of
 S. Garabet et al. / Field Crops Research 58 (1998) 213±221 217

Table 1 fertilizer was in the upper 20 cm soil layer; no ferti-

Labelled fertilizer nitrogen recovered in the 0±40 cm soil layer at lizer N was recovered below the 40 cm soil layer.
various sampling dates from the rain-fed or irrigated fertilized
(100 (kg N) haÿ1) plots
3.4. Nitrogen balance
Soil sampling date Fertilizer recovered in soila (kg haÿ1)

(days after sowing) NH‡

4 ±N NOÿ
3 ±N total N The fertilizer N recovery data were averaged for the
100 kg haÿ1 treatment replicates across irrigation
33 (rain-fed) 44 (28) 44 (13) Ð
137 (rain-fed) 10 (5) 10 (3) Ð levels (rain-fed and full irrigated) to provide a balance
210 (rain-fed) 6 (2) 15 (5) 56 (10) sheet (Fig. 3). Soil and plant 15N recoveries ranged
210 (irrigated) 1 (0.7) 2 (1) 43 (7) from 90 to 101%, with little difference between years.
37 (rain-fed) 91 (43) 13 (4) Ð Unrecovered N, which mainly includes N lost from the
117 (rain-fed) 57 (15) 9 (3) Ð
soil±plant system, ranged from 0 to 10% in each year.
184 (rain-fed) 18 (10) 12 (4) 73 (11)
184 (irrigated) 0.7 (0.3) 0.4 (0.2) 53 (7) Over half of the applied N remained in the soil, mostly
a
in the 0±20 cm soil layer. There was considerably
Mean of four replicates. Standard deviations are in parentheses.
more fertilizer N left in the rain-fed treatment than
in the irrigated treatments. Above 40% of the fertilizer
N recovered was in an inorganic form under rain-fed
100 (kg N) haÿ1. However, seasonal differences were conditions in both years, compared to <8% with
evident: in the drier year (117 days after sowing), most irrigation.
of the inorganic N was recovered as NH4±N, in
contrast to the wetter year (137 days after sowing), 3.5. Net soil N mineralization
where both NH4 and NO3±N were recorded in equal
amounts. Nitrogen recovered in fertilized soil (100 (kg To identify whether the lower fertilizer-use ef®-
N) haÿ1) after harvest (210 and 184 days after sowing ciency obtained in this study by the Direct method was
in Year 1 and Year 2, respectively) as total 15N was 56 actually due to added N interaction (Westerman and
and 43% for rain-fed and irrigated treatments, respec- Kurtz, 1973) or to mineralization±immobilization±
tively, in the wetter year, compared with 73 and 53% in turnover (Jenkinson et al., 1985), the net soil miner-
the drier year. In both years, >90% of the recovered alization of the total soil N (Table 2) was calculated

Fig. 3. Nitrogen balance sheet for nitrogen fertilizer (100 kg haÿ1) applied to wheat under rain-fed and irrigated conditions in two seasons.
218 S. Garabet et al. / Field Crops Research 58 (1998) 213±221

Table 2
Sources of nitrogen used by wheat at harvest, and net nitrogen mineralized from soil total nitrogen

Treatment Grain Total N Soil N Unrecovered N Source Net N

yield (t haÿ1) uptake (kg haÿ1) N mineralizeda
initial harvest fertilizer soil

1991/92
Rain-fed 2.8 55.1 52.5 33.2 Ð Ð 55.1 36.0
Rain-fed‡100 (kg N) haÿ1 3.2 106.0 52.5 58.8 0 44.8 61.2 12.2
Irrigated 3.6 66.4 52.5 28.4 Ð Ð 66.4 30.3
Irrigated‡100 (kg N) haÿ1 5.2 125.5 52.5 29.2 8 49.1 76.4 ÿ2.0
LSD (0.05) NW 13.3 11.4 22.6
1992/93
Rain-fed 1.56 34.9 64.2 22.8 Ð Ð 34.9 ÿ6.5
Rain-fed‡100 (kg N) haÿ1 1.65 66.3 64.2 74.3 2 24.5 41.8 ÿ22.0
Irrigated 3.20 55.4 64.2 19.6 Ð Ð 55.4 ÿ0.2
Irrigated‡100 (kg N) haÿ1 4.63 98.1 64.2 24.9 10 37.1 61.0 ÿ42.0
LSD (0.05) NW 12.2 11.4 16.9
a
Net N-mineralizedˆ[TNU ‡ soil inorganic-N at harvest ‡ N-loss] - [initial soil inorganic N ‡ N fertilizer applied ‡ addition through rain or
irrigation].

according to Hart et al. (1986) and Rao et al. (1992).
Fertilizer-N, unaccounted from the 15N balance, was
used as the N-loss and the amount of N added through
irrigation ranged from 11.2 to 11.9 (kg N) haÿ1. On
average, about 17 (kg N) haÿ1 more soil N was used
by wheat in the ®rst year. In both years, more soil N
was used by wheat in irrigated plots than in rain-fed
plots; the net-N mineralized in Year 1 was positive, but
negative values occurred in Year 2.
4. Discussion
Focussing on N ef®ciency and its measurements,
this paper complements the ®rst paper (Garabet et al.,
1998) which reported crop yields data from the same
experiment. Measurements of NFUE generally
showed that values recorded at harvest underestimate
fertilizer N-uptake ef®ciency, since this value was
greater at heading than at harvest in both years under
rain-fed conditions. This suggests that appreciable
amounts of N can be lost after heading, possibly
due to either leaf drop induced by water shortage in
rain-fed plots, or gaseous losses from plant tops (Mary
et al., 1987). Thus, NFUE values recorded are depen-
dent on the time or the growth stage selected for
evaluation of fertilizer recovery.
However, supplemental irrigation (particularly in a
relatively dry year) can reduce the decline in NFUE
after reaching a peak, by extending the life of green
leaves with longer photosynthetic activity. Thus, leaf
area index was greater and longer lasting in irrigated
than in rain-fed plants. Under the rain-fed Mediterra-
nean conditions of Syria, therefore, a relatively small
(<30 mm) supplemental irrigation at the sensitive
crop-growth period (before heading) can substantially
increase NFUE at harvest. Similar effects of moisture
on NFUE in wheat were demonstrated by others in the
region (Buresh et al., 1990; Soltanpour et al., 1987).
In accordance with other studies (Abdel Monem,
1986), NFUE values were low, and did not exceed
60% in either year, even under optimum N and
irrigation levels. Low recoveries of labelled ammo-
nium sulphate were also recorded by Pilbeam et al.
(1997) for rain-fed wheat growing at the same site in
Syria but at lower rates of 30 (kg N) haÿ1 applied at
autumn. Also, NFUE from the Difference method was
higher than that from the Direct method as shown by
Harmsen and Moraghan (1988) and Abdel Monem
(1986). As soil N differences between fertilized and
unfertilized plots were not signi®cant in either year,
mineralization±immobilization±turnover was prob-
ably responsible for the discrepancy between the
two methods (Jenkinson et al., 1985), with immobi-
lization being dominant over mineralization.
It was clear that limited moisture (probably induced
by the wheat/wheat compared to the less moisture-
demanding wheat/lentil sequence) and, therefore,
 S. Garabet et al. / Field Crops Research 58 (1998) 213±221
limited root exploitation (75 vs. 100 cm moisture pene-
tration) was a factor in explaining the higher NFUE in
the wetter year. The crop sequence in¯uences NFUE
in ways other than moisture availability. Legumes are
known to increase soil N levels whereas non-legumes
(i.e. cereals) usually provide little N bene®t (Giddens
et al., 1965), or they may induce net N immobilization
(Mahler and Hemamda, 1993) as in the second year of
this study: the 3-week delay in the sowing date may
have been also a factor in the lower ef®ciency values
obtained.
The high total fertilizer N recovered in soil and
plants which we observed coincides with previous
work at the same site (ICARDA, 1982), i.e. 95%
15
N recovery in Mexipak wheat and in the soil at
harvest. Also, fertilizer N loss was slightly smaller
than that calculated by Abdel Monem (1986) for urea
fertilizer at the same site (11±18%) and the 6±16%
observed by Feigenbaum et al. (1983). However,
Pilbeam et al. (1997) reported higher losses expressed
as a percentage of split-applied N (autumn and spring)
for rain-fed wheat. As fertilizer N did not leach
beyond 40-cm soil depth in the latter study, the
unaccounted N study was probably due to volatiliza-
tion.
As considerable amounts of fertilizer N remained in
the soil at harvest, immobilization appeared to be the
major process involved. With autumn fertilizer appli-
cation, as in this study, the long period prior to rapid
spring growth (e.g. from late November to early
March), when soil moisture is conducive to microbial
activity, may have promoted N immobilization. With
late fertilizer N application (i.e. in spring) soil micro-
bial needs are satis®ed by the native soil N so that a
higher percentage of fertilizer N remains available for
crops (Hart et al., 1986). The greater quantity of 15N-
fertilizer remaining as organic N in the 0±20 cm soil
layer in the irrigated plots suggests that higher immo-
bilization was stimulated by microbial activity under
the more favourable soil-moisture regime. Part of this
N was probably present in the crop root system, but
was unlikely to exceed 5±10% of the N in the above-
ground crop. However, recent estimates from foliar-
applied 15N for several ®eld crops in Australia showed
that below-ground N may represent 25±30% of total
crop N, e.g. lupins (Russell and Fillery, 1996).
With increased dry-matter production as well as
root size from tillering to anthesis, the rapid root
219
turnover may be an important source of rhizosphere
C, thus increasing the readily available C fraction for
microbial activity. Hence, the total amount of N
immobilized in the growing season is likely to
increase with increased N application as a result of
increased availability of organic C in the system. The
higher N immobilized and the lower net-N minera-
lized, calculated from the fertilized plots of this study,
con®rm this. However, the crop sequence probably
had a signi®cant in¯uence on the mineralization rate.
For example, we found relatively more net-N miner-
alized after a preceding lentil crop (Year 1) than after
wheat (Year 2), where net-N immobilization occurred.
Similarly, Myers and Paul (1971) found that the
addition of 448 (g wheat straw) mÿ2 increased net
fertilizer N immobilization by 1.3 (g N) mÿ2. The
low proportion of N mineralization from wheat resi-
dues can be attributed to their high C/N ratio (Bremner
and Van Kissel, 1992).
Mineralization of the immobilized fertilizer N
obviously did not take place in this study since the
amount of N derived from fertilizer measured in the
soil did not increase any time during the two years.
Shen et al. (1989) showed that the re-mineralization of
labelled-N, which is immobilized within a short period
of a few days or weeks, is very slow, even occurring
over several years. Thus, residual immobilized
fertilizer N is primarily a long-term source of N for
crops; it builds up soil organic N with a bene®cial
effect. This means that, under the Mediterranean
conditions where N losses are relatively low, NFUE
is, to a large extent (Mary et al., 1987), determined by
competition between the immobilization process and
plant uptake.
5. Conclusions
This study indicated that under the rain-fed wheat-
growing Mediterranean conditions in Syria, recovery
is <50% of the applied fertilizer N. Immobilization
within the current season is a main cause of unused
fertilizer N, considerable amounts of which remain in
the soil in organic form. However, continued accu-
mulation of fertilizer N in the topsoil is not a real loss,
as immobilized N improves soil fertility and reduces
fertilizer N requirements in subsequent years. Addi-
tionally, supplemental irrigation can improve fertili-
220 S. Garabet et al. / Field Crops Research 58 (1998) 213±221
zer-N ef®ciency. Management practices (e.g. suitable
sowing date, proper rotation, supplemental irrigation,
splitting fertilizer N if suitable rainfall conditions
prevail) that lead to both, lower fertilizer N immobi-
lization and higher plant N uptake ± and thus higher
NFUE values, would be bene®cial. The method by
which NFUE is calculated can also have a consider-
able effect. The mineralization±immobilization±turn-
over process and the added N interaction can cause
uncertainty when N ef®ciency is measured by the
Difference or the Direct method, due to either real
N interaction or biological exchange between soil and
fertilizer N by mineralization±immobilization±turn-
over. These processes may occur simultaneously,
being dif®cult to separate from each other. Never-
theless, as N interaction was not evident in this study,
we conclude that mineralization±immobilization±
turnover is the dominant process that controls the
soil±plant N dynamics. In this context, studies using
15
N-labelled fertilizer can de®ne the precise amount of
fertilizer N in the plant and the soil and, particularly,
the amount lost from the system.
Acknowledgements
We express our appreciation to Drs. Lester Sim-
monds, Abdallah Matar and Douglas Beck for their
advice in planning of this work. We also appreciate the
technical support of several ICARDA and Reading
University staff in the ®eld and laboratories.
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