Grain yield, efficiency and the allocation of foliar N applied to soybean canopies

Abstract

Soybean [Glycine max (L.) Merr.] grain yield is closely associated with the level of
optimal nitrogen (N) supply, especially during the reproductive stages. Foliar fertilization with low
rates of N have been considered as a strategy for furnishing additional N and enhancing grain
yields. Field studies using 15N tracer were conducted over two growing seasons to investigate
the impact of foliar N fertilization on grain yield, plant N content, the amount of N derived from
fertilizer (NDFF) and N recovery efficiency (NRE). Four foliar N rates (0, 1300, 2600 and 3900 g
ha–1) were supplied by two equal split applications at the R1 and R3 stages. Foliar N fertilization
of soybean canopies did not affect grain yield, grain N content, shoot N content nor plant N
content. Total NDFF was increased from 0.7 to 2.0 kg ha–1 across the N rates. Nonetheless,
NRE was unaffected by foliar N fertilization, which averaged 53 %. Soybean plants allocated the
same amount of N fertilizer to both grains and shoots. No significant effects of low rate foliar N
fertilization were registered on soybean grain yield nor plant N content, despite considerable N
fertilizer recovery by plant organs.

Full text

DOI: http://dx.doi.org/10.1590/1678-992X-2017-0395
Sci. Agric. v.76, n.4, p.305-310, July/August 2019
ISSN 1678-992X
ABSTRACT: Soybean [Glycine max (L.) Merr.] grain yield is closely associated with the level of
optimal nitrogen (N) supply, especially during the reproductive stages. Foliar fertilization with low
rates of N have been considered as a strategy for furnishing additional N and enhancing grain
yields. Field studies using 15N tracer were conducted over two growing seasons to investigate
the impact of foliar N fertilization on grain yield, plant N content, the amount of N derived from
fertilizer (NDFF) and N recovery efficiency (NRE). Four foliar N rates (0, 1300, 2600 and 3900 g
ha–1) were supplied by two equal split applications at the R1 and R3 stages. Foliar N fertilization
of soybean canopies did not affect grain yield, grain N content, shoot N content nor plant N
content. Total NDFF was increased from 0.7 to 2.0 kg ha–1 across the N rates. Nonetheless,
NRE was unaffected by foliar N fertilization, which averaged 53 %. Soybean plants allocated the
same amount of N fertilizer to both grains and shoots. No significant effects of low rate foliar N
fertilization were registered on soybean grain yield nor plant N content, despite considerable N
fertilizer recovery by plant organs.
Keywords: Glycine max (L.) Merr, foliar N fertilization, 15N tracer, foliar application, nitrogen
recovery efficiency
Grain yield, efficiency and the allocation of foliar N applied to soybean canopies
Silas Maciel de Oliveira1* , Clovis Pierozan Junior2, Bruno Cocco Lago1, Rodrigo Estevam Munhoz de Almeida3, Paulo Cesar
Ocheuze Trivelin4, José Laércio Favarin1
1Universidade de São Paulo/ESALQ – Depto. de Produção
Vegetal, Av. Pádua Dias, 11 – 13418-900 – Piracicaba,
SP – Brasil.
2Instituto Federal de Educação, Ciência e Tecnologia do
Paraná, Av. Bento Munhoz da Rocha Neto, 280 – 85555-000
– Palmas, PR – Brasil.
3Embrapa Pesca e Aquicultura, C.P. 90 – 77008-900 –
Palmas, TO – Brasil.
4Universidade de São Paulo/CENA – Lab. de Isótopos
Estáveis, Av. Centenário, 303 – 13416-000 – Piracicaba,
SP – Brasil.
*Corresponding author <silasmaciel@usp.br>
Edited by: Richard L. Mulvaney
Received November 23, 2017
Accepted February 24, 2018
Introduction
Foliar nitrogen (N) fertilization is an increasingly
common practice in commercial grain soybean [Gly-
cine max (L.) Merr.] production. Soybean N fixation will
necessarily reflect variations in soil N supplying power,
and although soybeans can fix appreciable amounts of
N ~200 kg ha–1 (Unkovich and Pate, 2000; Alves et al.,
2003; Herridge et al., 2008), recent studies document
that N limits grain yield (Wilson et al., 2014; Felipe et
al., 2016). The application of low amounts of N as a fo-
liar spray is a pathway for additional N, especially dur-
ing the pod-filling stage when N demand is high (Gaspar
et al., 2017). In addition, compatibility with pesticides
commonly applied reduces costs and more foliar N ap-
plications may be performed.
Previous studies have shown grain yield increases
resulting from foliar N fertilization (Vasilas et al., 1980;
Blandino and Reyneri, 2009; Ranđelović et al., 2009; Jyo-
thi et al., 2013; Khan et al., 2013). It has been suggested
that foliar N application may provide other advantages
as well. Using foliar N application during the pod-filling,
Ikeda et al. (1991) reported increased photosynthetic
productivity in leaves and the export of photosynthates
to the nodules for an extended length of time. In studies
investigating foliar application effects on grain N con-
centrations, such concentrations increased between 0.2
% and 2.4 % (Ruske et al., 2003; Blandino and Reyneri,
2009; Mandić et al., 2015).
In contrast, a lack of grain yield effect has also
been observed in many field studies. Excessive foliar
damage may limit grain yield responses when high rates
of N are applied under leaves (Phillips and Mullins,
2004). However, two reviews performed by Gooding and
Davies (1992) and Fageria et al. (2009) showed that grain
yield responses are also closely correlated with foliar ap-
plication timing. The same authors observed that grain
yield increases were most commonly obtained through
foliar application during the reproductive stages and
with negligible foliage burning.
While these studies provide valuable information
about foliar N fertilization, only a few studies have in-
vestigated foliar fertilizer recovery efficiency in soybean
crops. Moreover, previous studies have involved higher
rates of foliar N fertilizer than are used in Brazilian soy-
bean production to supply N while avoiding leaf dam-
age. Knowledge of foliar N recovery efficiency (NRE)
and its allocation in soybean crops could help to better
implement foliar N application strategies and to better
understand the effects on grain yield. Therefore, using
15N tracer methods, the main goal of this study was to
investigate the effects of foliar N fertilization on grain
yield and NRE.
Materials and Methods
Site description
The field experiment was performed in the state of
São Paulo (49°15’08” W, 23°34’53.5” S, 545 m asl) over
two growing seasons in 2012-2013 (Year 1) and 2013-
2014 (Year 2). Located in the southwest of Brazil, this
experimental area has a subtropical humid climate (Köp-
pen, 1936) with low seasonal precipitation variation.
The rainfall and mean temperature for crop seasons are
shown in Figures 1A and B. Based on the USDA (1999)
classification system the soil is classified as a Typic Hap-
Crop Science | Research Article

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Sci. Agric. v.76, n.4, p.305-310, July/August 2019
ludalf with 657 g kg–1 clay, 253 g kg–1 silt and 190 g kg–1
sand. Before planting, the soil chemical properties were
measured at a 0-20 cm depth, and provided the follow-
ing results: pH of 5.5 (CaCl2), 40 g of organic matter
dm–3, 2.2 g of N kg–1, P (resin extractable) of 19 mg kg–1,
exchangeable K of 0.76cmolc kg–1 and base saturation of
70 %.
The experiment was conducted using a random-
ized block design with four replicates. Treatments con-
sisted of four foliar N rates (0, 1300, 2600 and 3900 g
ha–1) applied as urea through two equal split applications
at R1 and R3 stages (Fehr and Caviness, 1977). No fo-
liage burning was noted across the applications. Each
plot consisted of 10 m-long rows spaced 0.45 m apart.
The Nideira 5909 RR variety was planted at 226,000 and
247,000 seeds ha–1 for years 1 and 2, respectively. Phos-
phorus and potassium were applied in the furrow during
planting as triple superphosphate (86 kg ha–1 P2O5) and
KCl (65 kg ha–1 K2O).
N internal efficiency (NIE) indicates how efficiently
soybean grains produce relative to the N accumulated by
the aboveground biomass (kg grain produced/kg aboveg-
round biomass N content) (Fageria, 2014).
Foliar N fertilizer was applied using a manual back-
pack sprayer pressurized with CO2 and equipped with a
flat spray tip applying a 200 L ha–1 spray volume. The
soybean canopy was situated 0.5 m below the spray tip.
15N methods
Each treatment plot, a microplot with four 1 m
rows and a total area of 1.8 m2 received labeled fertil-
izer spread containing 2.53 atom % 15N, according to the
rates and stages described earlier. The remaining plants
in the plot were treated with unlabeled fertilizer.
Labeled samples were taken at the R7 stage (Fehr
and Caviness, 1977) to evaluate the total N and the N
derived from fertilizer (NDFF) amounts in the soybean
biomass above ground. Four plants were collected from
each of the two rows in the middle of the microplots
and divided into grain and shoot categories (petiole,
leaf, steam and pod). This early sample aimed to avoid
leaf drop and increase the non-recovery of 15N (NRN).
Grain yield was obtained using unlabeled samples taken
at physiological maturity and by adjusting the moisture
level to 130 g kg–1. Approximately 100 plants were col-
lected within 3 m of the three central rows of each plot.
All samples were dried in a forced air circulation
laboratory oven at 65 °C, weighed and carefully ground
into fine powder using a Wiley mill. The 15N/14N ratios as
well as the total N concentration in plant samples were
determined in an automated mass spectrometer coupled
to an ANCA-GSL N analyzer (Sercon Co., UK). The term
N recovery efficiency (NRE) was used to indicate the
percent of N fertilizer recovery by the whole plant. The
NDFF was used to indicate the amount of N fertilizer
recovery in compartments of the whole plant, expressed
in kg ha–1. NDFF values were obtained using the follow-
ing equation.
NDFF (kg ha–1) =
αβ
γβ
−
−




. total N (1)
where: NDFF is the amount of N derived from the fer-
tilizer (kg ha–1), α the abundance of 15N atoms in the
sample (%), β the natural abundance of 15N atoms, γ the
abundance of 15N atoms in the fertilizer (2.53 % atoms),
and total N the total N (15N+14N) contained in the sam-
ple (kg ha–1).
NRE (%) = Total NDFF
N rate




. total N (2)
where: NRE is the percentage of 15N recovered from the
whole soybean plant, Total NDFF the amount of 15N re-
covered from whole plant (kg ha–1), and the fertilizer N
rate the rate of enriched fertilizer applied (kg ha–1).
Statistical analyses
All data were analyzed using the statistical soft-
ware program (SAS v. 9.2, 2009). Before analysis, the
observations from the response variables were tested
for homoscedasticity using the Box-Cox test (Box and
Cox, 1964). F-tests were performed at a 5 % probabil-
ity to identify the effects and their interactions. If the
null hypothesis was rejected, the mean was compared
via Fisher’s least significant difference (LSD) test at p ≤
0.05 probability, and regressions were fitted to the rates
when necessary.
Results
Foliar N fertilization had no effect on grain yield
(Table 1) and yield components such as the number of
nodes, pods, stems or seed weight (data not shown).
Figure 1 – Rainfall and average air temperature during the soybean
growing season in 2012-13 (A) and 2013-14 (B). Planting and
growth stages are specified in accordance with Fehr and Caviness
(1977).

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NDFF was significantly different across the rates and
ranged from 0.32 to 0.83 kg ha–1 (Figure 2B).
As noted for grains and shoots, total NDFF was sig-
nificantly affected by rates. Despite the year difference,
there was no interaction effect between year and rate.
Our regression analysis showed that total NDFF increased
~0.5 g N kg–1 when N fertilizer was applied (Figure 2C).
There was no difference between the rates of fo-
liar N applied for NRE. Even though the years differed,
the interaction between year and rate was not signifi-
cantly affected (Table 2 and Figure 2D). On average,
NRE was 53 % for foliar N applications performed on
soybean canopies.
N fertilizer distribution is shown in Figures 3A and
B. Except for the higher rate in year 1, the same amounts
of N fertilizer were allocated in the grains and shoots
(p > 0.05). Overall, shoot recovery ranged from 18 % to
27 % and grain recovery ranged from 21 % to 42 %.
Nonetheless, we registered differences between grain
years. Grain yield means were 3.7 and 4.2 Mg ha–1 for
years 1 and 2, respectively. Plant N content and NIE
had similar responses to foliar N application, and while
no difference was registered across rates, differences be-
tween years were significant for grain and plant N con-
tent. Grain and plant N content ranged between 185-197
kg ha–1 and 254-281 kg ha–1, respectively, throughout the
two years of the study. Average shoot N content was 79
kg ha–1.
As might be expected, high rates of foliar N re-
sulted in greater grain NDFF. There were statistical dif-
ferences between years (Year 1 > Year 2), but no inter-
action between year and rate (Table 2). A positive linear
regression between grain NDFF and rates was fitted
(Figure 2A).
There was no difference in NDFF between years
and their interaction with rates. Nevertheless, the shoot
Table 2 – Grain, shoot and total N derived from fertilizer (NDFF) and N recovery efficiency (NRE) for different years and rates.
Treatment Rate NDFF NRE
Grain Shoot Plant
g ha–1 -------------------------------------------------------------------- kg ha–1 -------------------------------------------------------------------- %
1300 0.35 0.32 0.68 52.0
2600 0.76 0.65 1.42 54.3
3900 1.21 0.83 2.04 52.3
Years
Year 1 0.99 A 0.64 1.63 A 60.8 A
Year 2 0.57 B 0.56 1.13 B 44.9 B
Average
0.78 0.60 1.38 52.9
ANOVA Pr > F
Year (Y) *** ns * *
Rate (R) *** *** *** ns
Y*R ns ns ns ns
CV % 16.7 12.3 13.8 10.5
*Significance at p ≤ 0.05; ***Significance at p ≤ 0.001; ns = not significant. Within lines, means followed by different letters are significantly different.
Table 1 – Grain yield, N internal efficiency (NIE), and N content for grain, shoot and plant for different years and rates.
Treatment Rate Grain yield NIE Grain N content Shoot N content Plant N content
g ha–1 Mg ha–1 --------------------------------------------------------------------------------------- kg ha–1 ----------------------------------------------------------------------------------------
0 3.98 15.9 185 69 254
1300 3.88 13.6 196 85 281
2600 4.00 15.0 192 86 279
3900 4.07 14.2 197 76 273
Years
Year 1 3.74 B 14.9 174 B 80 254 B
Year 2 4.22 A 15.0 211 A 78 289 A
Average
3.98 15.0 192 79 271
ANOVA Pr > F
Year (Y) * ns * ns *
Rate (R) ns ns ns ns ns
Y*R ns ns ns ns ns
CV % 8.81 5.94 18.1 20.3 16.4
*Significance at p ≤ 0.05; ns = not significant. Within lines, means followed by different letters are significantly different.

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Discussion
Differences between years for grain yield may be a
combination of a slight increase (~8 %) of planting rate in
year 2 (De Bruin and Pedersen, 2008; Cox and Cherney,
2011), accompanied by better growing conditions (Fig-
ure 1A and B). However, N provided by low rates of fo-
liar applications showed no differences in soybean grain
yield. Previously reported in the literature, Troedson et al.
(1989) and Haq and Mallarino (2000) showed that foliar N
fertilization effects on grain yield were usually insignifi-
cant. Recently, despite high grain yields (> 4.2 Mg ha–1),
Saturno et al. (2017) and Moreira et al. (2017) have found
similar results to those in this study using foliar N rates
ranging from 5-20 kg ha–1 and 5-10 kg ha–1, respectively.
For the same studies, only one out of five year sites had
significant, but small, grain yield gains (~0.14 Mg ha–1).
Our results agree with the lack of effects of foliar
N fertilization on grain yield previously found in litera-
ture, but also showed that the lack of effect on grain
yield is not linked to low efficiency of fertilizer applica-
tion since approximately 53 % of the foliar N fertilizer
was recovered. Rather, the implication is that low rates
of foliar N were of no benefit to the soybean crop, either
for directly supplying N or indirectly increasing green
leaf area index.
For soybeans, NIE values ranging from 6.4 to 18.8
and with a mean of 12.7 have been reported (Salvagiotti
et al., 2008 and references cited therein). Mid to upper
NIE values indicate N is the main limiting factor for
grain yield. Thus, our results reflect higher NIE (~15)
when compared with historical means, demonstrating
that the low rates of foliar N might not be enough to
support N demand. However, it is not clear how much
exogenous N would be the optimal to achieve greater
grain yields.
While there was an appreciable increase in NDFF
(amount of fertilizer recovery) for all rates, the NRE (per-
cent of fertilizer recovery) was similar, with an average
value of 53 % (Figure 2A, B and C). The NRE was com-
parable to that previously reported by Afza et al. (1987),
which was 43-67 % of the total foliar N applied. In a re-
cent study investigating the effects of low rates of foliar
N fertilization on soybeans (Pierozan Junior et al., 2015),
the authors show a mean NRE of 64 % that was not af-
fected by rates ranging from 650 to 1950 g N ha–1. Thus,
foliar N fertilization was an efficient pathway to supply N
in soybean plants, despite its lack of effect on grain yield.
Figure 2 – Foliar N rates effects on grain (A), shoot (B), total NDFF (C) and NRE (D). N derived from fertilizer, NDFF and N recovery efficiency,
NRE. **Significance at p ≤ 0.01; ***Significance at p ≤ 0.001.
Figure 3 – Allocation of N fertilizer sprayed under soybean leaves.
Year 1 (A) and Year 2 (B). Uppercase letters indicate significant
difference between organs for the same foliar N rate.

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Generally, our results showed that foliar N fertil-
ization had little to no effect on 15N partitioning. The
lack of differences between grains and shoots could be
attributed to N investment in the leaf blends and their
photosynthesis rates (Makino et al., 1997). When the N
was applied between the R1 and R3 growth stages, the
grain sink capacity remained low to medium, but rubis-
co and light harvesting proteins had a high N demand.
Accordingly, Vasilas et al. (1980) reported up to 94 % 15N
allocation in the grain when spraying foliar N as urea at
the R5-R7 growth stages.
Conclusions
The NRE had no effect across all the foliar N rates
and 53 % of N sprayed under leaves was recovered.
Overall, grains and shoots allocated N from fertilizer
equally well and recovered 29 % and 24 %, respectively.
Despite the considerable recovery of N supplied to soy-
bean plants, low rates of N sprayed in the earlier pod-
filling stage was not an effective method for enhancing
grain yield and dynamic N uptake. The foliar N fertiliza-
tion effect is not fully understood and is worth further
study, especially during pod-filling.
Acknowledgments
Funding was provided by Stoller do Brasil Ltda.
The funders had no role in data collection and analysis,
decision to publish, or preparation of the manuscript.
We thank José Luiz Motta de Almeida and his staff for
logistical support. The authors would also like to ackno-
wledge the Fundação de Amparo à Pesquisa do Estado de
São Paulo (FAPESP, 2012/24266-5), the Conselho Nacio-
nal de Desenvolvimento Científico e Tecnológico (CNPq,
141444/2014-2) and the Coordenação de Aperfeiçoamento
de Pessoal de Nível Superior (CAPES, 8881.134205/2016-
01) for providing graduate scholarships.
Authors’ Contributions
Conceptualization: Maciel de Oliveira, S.; Almeida
R.E.M; Pierozan Junior, C. Data acquisition: Maciel de
Oliveira, S.; Almeida R.E.M; Pierozan Junior. C.; Lago,
B.C. Data analysis: Maciel de Oliveira, S. Design of Me-
thodology: Maciel de Oliveira, S.; Almeida R.E.M; Pie-
rozan Junior. C.; Lago, B.C.; Trivelin; P.C.O. Software
development: Maciel de Oliveira, S. Writing and editing:
Maciel de Oliveira, S.; Almeida R.E.M; Pierozan Junior,
C.; Favarin, J.L.
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