Engenharia Agrícola

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Scientific Paper
Doi: http://dx.doi.org/10.1590/1809-4430-Eng.Agric.v42n2e20210177/2022

REMOTE DETECTION OF WATER AND NUTRITIONAL STATUS OF SOYBEANS

USING UAV-BASED IMAGES

Aderson S. de Andrade Junior1*, Silvestre P. da Silva2, Ingrid S. Setúbal2,

Henrique A. de Souza1, Paulo F. de M. J. Vieira1
1*
Corresponding author. Embrapa Meio-Norte/ Teresina - PI, Brazil.
E-mail: [email protected] | ORCID ID: https://orcid.org/0000-0002-0619-1851

KEYWORDS ABSTRACT
Glycine max L., RPA, Digital aerial images obtained by cameras embedded in remotely piloted aircraft (RPA)
vegetation indexes, have been used to detect and monitor abiotic stresses in soybeans, such as water and
gas exchange. nutritional deficiencies. This study aimed to evaluate the ability of vegetation indexes
(VIs) from RPA images to remotely detect water and nutritional status in two soybean
cultivars for nitrogen. The soybean cultivars BONUS and BRS-8980 were evaluated at
the phenological stages R5 and R3 (beginning of seed enlargement), respectively. To do
so, plants were subjected to two water regimes (100% ETc and 50% ETc) and two
nitrogen (N) supplementation levels (with and without). Thirty-five VIs from
multispectral aerial images were evaluated and correlated with stomatal conductance (gs)
and leaf N content (NF) measurements. Near-infrared (NIR) spectral band, enhanced
vegetation index (EVI), soil-adjusted vegetation index (SAVI), and renormalized
difference vegetation index (RDVI) showed linear correlation (p<0.001) with gs, standing
out as promising indexes for detection of soybean water status. In turn, simplified canopy
chlorophyll content index (SCCCI), red-edge chlorophyll index (RECI), green ratio
vegetation index (GRVI), and chlorophyll vegetation index (CVI) were correlated with NF
(p<0.001), thus being considered promising for the detection of leaf N content in soybeans.

INTRODUCTION status, the incidence of pests and diseases, weed infestation,

and productive potential (Tetila et al., 2017; Franchini et al.,
According to precision agriculture principles, high-
2018; Barbedo, 2019).
precision and low-cost estimates of plant biophysical and Drought stress has reduced global soybean yields by
biochemical parameters are important to improve more than 50% annually (Wang et al., 2003). The effect of
management practices and productive potential in farming droughts on soybean yields depends on the severity,
systems (Vibhute & Bodhe, 2012). High throughput and duration, and timing of stress regarding the crop growth
spatial accuracy of these estimates using aerial images from stage (Brar et al., 1990). Soybean is most susceptible to
remotely piloted aircraft (RPA) can assist in evaluating drought stress during its reproductive stage (Wijewardana
genotype behavior, management practices, and impacts of et al., 2018, 2019b); however, when under long-term severe
biotic and abiotic stresses, thus contributing to decision- water stress during vegetative growth, substantial yield
making by farmers (Franchini et al., 2018). losses can be caused (Machado et al., 2020).
Digital aerial images from RPAs have been used to Drought effects on soybean physiological and
detect and monitor spatial and temporal variability in biochemical changes are not clearly understood yet
croplands (Barbedo, 2019). Studies have demonstrated the (Manalavan et al., 2009). Soil moisture stress may induce
viability of aerial images at some crop development stages several morpho-physiological and biochemical responses
to spatialize information about vegetative vigor, nutritional that subsequently inhibit growth, lower photosynthesis,

1 Embrapa Meio-Norte/ Teresina - PI, Brazil.

2 Programa de Pós-graduação em Agronomia - Universidade Federal do Piauí/ Teresina - PI, Brazil.
Area Editor: Fabio Henrique Rojo Baio
Received in: 9-23-2021
Accepted in: 4-7-2022
Engenharia Agrícola, Jaboticabal, v.42, n.2, e20210177, 2022
Edited by SBEA
Aderson S. de Andrade Junior, Silvestre P. da Silva, Ingrid S. Setúbal, et al.

reduce stomatal conductance and transpiration, decrease Given the above, we hypothesize that soybean water
chlorophyll contents, and cause changes in proteomics and nutritional status can be detected using vegetation
(Reddy et al., 2004; Wijewardana et al., 2019a). indexes from aerial images derived from multispectral
Leaf nitrogen (N) contents are directly correlated cameras embedded in RPAs. Thus, this study aimed to
with chlorophyll production, thus affecting crop growth and evaluate the ability of vegetation indexes from aerial images
yield. Farmers have used soil plant analysis development of a multispectral camera embedded in a remotely piloted
(SPAD) devices to estimate chlorophyll contents in plants. aircraft (RPA) to remotely detect the water and nutritional
However, large-scale crop monitoring through SPAD is status of two soybean cultivars regarding N contents.
time-consuming and demanding; therefore, unmanned
aerial vehicles (UAV) are recommended for estimating leaf MATERIAL AND METHODS
N contents in crops using multispectral imagery (Colorado The experiment was conducted in the experimental
et al., 2020). area of Embrapa Meio-Norte in Teresina, PI, Brazil (05°05'
Some studies have been conducted on the use of S, 42°49' W, and 74.4-m altitude), from July to November
aerial images to detect and monitor abiotic stresses, 2019 (Figure 1). The historical annual averages of
especially water and nutritional stresses in soybeans temperature and cumulative rainfall are 27.4 °C and 1,325
(Hoyos-Villegas & Fritschi, 2013; Yu et al., 2016; mm, respectively, with rains concentrated between January
Maimaitijiang et al., 2017; Franchini et al., 2018; and May (INMET, 2019). During the experiment, mean
Wijewardana et al., 2019b). Regarding nutritional status, maximum and minimum temperatures and cumulative
Franchini et al. (2018) studied soybean spectral responses rainfall were 29.44 °C, 27.6 °C, and 0.11 mm, respectively
to potassium (K) application and observed a correlation (INMET, 2019). The local climate is defined as Aw
between K levels in the soil and modified photochemical according to the Köppen classification, with a rainy season
reflectance index (mPRI). in the summer and a dry season in the winter (Medeiros et
Remote detection of water deficit in crops can be al., 2020). The soil in the experimental area is classified as
performed by the joint use of vegetation indexes, such as eutrophic Red Yellow Argisol (Melo et al., 2014) (Table 1).
NDVI, and leaf canopy temperature measurements from The experiment was carried out using two soybean
thermal cameras embedded in RPAs (Carvalho et al., 2015; cultivars: 1) BONUS, with indeterminate growth habit,
Hoffmann et al., 2016; Crusiol et al., 2017; Sagan et al., maturity group (MG) 7.9, a cycle of 105-122 days; and 2)
2019; Crusiol et al., 2020). Crusiol et al. (2020) evaluated BRS-8980, with determinate growth habit, MG 8.9, and a
the use of remote (hyperspectral) and airborne (RGB/NIR cycle of 125-136 days. The design adopted was a
and thermal cameras embedded in drones) sensors to detect randomized block arranged in a split-plot scheme, in which
water deficit in soybeans. They concluded that remote plots comprised two water regimes (WR): deficit irrigation
sensors could differentiate water conditions in soybean (50% crop evapotranspiration [ETc] replacement) and full
cultivars, improving management and decision-making in irrigation (100% ETc replacement), while subplots
terms of crop practices. consisted of two nitrogen (N) supplementation levels (NS):
Some vegetation indexes (VIs) from multispectral without N (N0) and with N (N1; 1,000 kg ha-1). Therefore,
images are related to crop water status (Gago et al., 2015). four treatments (I0N0, I0N1, I1N0, and I1N1) were
Baluja et al. (2012) found a significant correlation between performed, with five replicates each.
VIs from multispectral imagery (e.g., NDVI and OSAVI) Sowing was performed manually on July 23, 2019,
and vine water stress indexes (e.g., stomatal conductance). by distributing 20 seeds per meter along furrows. Before
Likewise, Wijewardana et al. (2019b) evaluated the use of sowing, seeds were inoculated with Bradyrhizobium
vegetation indexes to detect water status in soybeans and japonicum (SEMIA 5079 and 5080) at a ratio of 100 mL
concluded that NDVI has a high positive linear correlation inoculant to 7 kg seeds. After germination, seedlings were
with leaf water potential and stomatal conductance. thinned out, leaving 10 to 12 plants per meter. For the
However, the use of multispectral indexes with cultivar BONUS, each plot contained twenty 6-m rows
physiological and thermal indicators of plant water status spaced 0.5 m apart (60 m²) and a 24-m² useful area. For the
still needs validation to replace aerial thermography, which cultivar BRS-8980, each plot contained twenty 4.5-m rows
is more expensive (Bian et al., 2019). spaced 0.5 m apart (45 m²) and an 18-m² useful area.

Engenharia Agrícola, Jaboticabal, v.42, n.2, e20210177, 2022

Remote detection of water and nutritional status of soybeans using UAV-based images

FIGURE 1. Location (A) and detailing (B) of the experimental area. Teresina, PI, 2019.

TABLE 1. Chemical properties and soil granulometry of the experimental area. Teresina, PI, 2019.

Depth Sand Fine Sand Silt Clay Textural Classification

Layer (m) -1
--------------------------- g kg ----------------------------
0.0-0.2 267.3 470.6 116.0 146.1 Loam-sandy
0.2-0.4 231.6 424.0 105.5 238.9 Loam-clay-sandy
Depth Layer P K Ca Mg H+Al SB CEC OM S
pH (CaCl2)
(m) mg/dm³ ---------------------- cmolc/dm³ -------------------- dag/kg %
0.0-0.2 10.15 0.23 2.40 0.83 1.18 3.45 4.63 1.03 74.5 5.50
0.2-0.4 5.41 0.22 2.63 0.83 1.34 3.68 5.01 0.91 73.4 5.38
P: phosphorus; K: potassium; Ca: calcium; Mg: magnesium; H+Al: potential acidity; SB: sum of bases; CEC: cation exchange capacity; OM:
organic matter; V%: base saturation; pH (CaCl2): pH in calcium chloride.

Fertilization was managed based on the soil estimated reference evapotranspiration (ETo) and soybean
chemical analysis. Nitrogen (urea), phosphorus (simple FAO crop coefficients – Kc (Allen et al., 1998). Climatic
superphosphate), and potassium (potassium chloride) were data (global solar radiation [MJ m-2], air temperature [°C],
applied to the soil, while micronutrients were sprayed on relative air humidity [%], and wind speed [ms-1]) were
leaves (Silva, 2021). The dose of 1,000 kg N ha-1 was acquired from an automatic agro-meteorological station,
selected to meet soybean N demands throughout the crop which is 500 m away from the experimental area. Irrigation
season so that both cultivars could express their maximum was performed using a fixed conventional sprinkler system,
yield potentials (6 Mg ha-1 expected yield). To that end, for with 24 sprinklers spaced at 12 m x 12 m. Irrigation depth
each Mg soybean produced, 80 kg N ha-1 were estimated, at was controlled by installing two blocks of 12 collectors
an N fertilization efficiency of 50% (Hungria et al., 2001). each, one for each water regime (WR), spaced 3 m between
Irrigation was managed to replace crop lateral sprinkler lines and in the center of the experimental
evapotranspiration (ETc), using the Penman-Monteith area. Soil moisture was monitored using Campbell’s CS616

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Aderson S. de Andrade Junior, Silvestre P. da Silva, Ingrid S. Setúbal, et al.

soil moisture probes, with three rods for each WR, two for bands simultaneously: blue (475 nm), green (560 nm), red
the 0.0-0.3 m and one for the 0.3-0.6 m depth layers, with (668 nm), Red Edge (717 nm), and NIR (840 nm). The
continuous measures recorded in a CR1000 datalogger. generated images were georeferenced and corrected using
WRs were applied as a function of soybean GPS and a solar radiation sensor installed on the top of the
development stages (Thomas, 2018 adapted from Fehr & aircraft, respectively. A radiometric calibration standard
Caviness, 1977). From sowing to stage V3 (three main stem was also used to correct the images, which were saved in
nodes with fully developed leaves), irrigation was fully 16-bit tiff format. Then, orthomosaic images were created,
applied in both treatments (100% ETc). Thereafter, from V4 using the Pix4D Mapper® software.
(four main stem nodes with fully developed leaves) to R5 The orthomosaic generated underwent a supervised
(beginning of seed enlargement), both WRs were performed, classification process (maximum likelihood method),
namely replacing 50 and 100% ETc. After R5, irrigation was allowing the rasterization of the orthomosaic into two
again fully applied in both treatments (100% ETc). classes (soil and leaves). This enabled the removal of pixels
The imagery was acquired from a hexacopter classified as mosaic soil, ensuring that the VIs had been
unmanned aerial vehicle (UAV), model X800, produced by estimated only with pixels classified as leaves. The process
XFly Brasil (XFly Tecnologia, Bauru, Brazil). A flight was was performed using the Semi-Automatic Classification
performed on September 24, 2019, 62 days after soybean
(SCP) plug-in of QGIS v. 218 (QGIS, 2016).
sowing - DAS (at R5 stage for BONUS and R3 for BRS-
The spectral responses of soybeans to the treatments
8980), between 11:00 am and 12:00 pm. The flight was
planned using the software Pix4D Capture® were quantified using 35 VIs from multispectral image
(www.pix4d.com) to ensure image capture with 80% side bands (R, G, B, Red Edge, and NIR) (Table 2). The
and front overlap. The flight line was maintained at 30 multispectral indexes were estimated using the QGIS raster
meters above ground level, with a GSD (ground sample calculator (QGIS, 2016). The VI values of each subplot
distance) of ≈ 1.5 cm. were extracted with the QGIS zonal statistics plugin (QGIS,
Multispectral images were acquired by a Micasense 2016). To this end, the vector layer of the subplots was used,
sensor, model RedEdge®, capable of capturing five spectral containing only the areas classified as leaves.

TABLE 2. Spectral bands and vegetation indexes evaluated in the study.

Band/Index Acronym Equation Reference

Green band GREEN / /
Red band RED / /
Red-Edge band RED-EDGE / /
NIR band NIR / /
𝑅
Chlorophyll index red CI-RED −1 Gitelson et al. (2005)
𝑅
𝑅 𝑅
Chlorophyll vegetation index CVI Vincini et al. (2008)
𝑅
2.5(𝑅 − 𝑅 )
Enhanced vegetation index EVI Huete et al. (2002)
𝑅 + 6𝑅 − 7.5𝑅 + 1
2.5(𝑅 − 𝑅 )
Two-band enhanced vegetation index EVI2 Jiang et al. (2008)
𝑅 + 2.4𝑅 + 1
3𝑅 − 2.4𝑅 − 𝑅 Meyer & Camargo Neto
Excess green red EXGR
𝑅 +𝑅 +𝑅 (2008)
𝑅
Green chlorophyll index GCI −1 Gitelson et al. (2005)
𝑅
2𝑅 − 𝑅 − 𝑅
Green leaf index GLI Hunt et al. (2013)
2𝑅 + 𝑅 + 𝑅
Green normalized 𝑅 −𝑅
GNDVI Hunt e Daughtry (2018)
difference vegetation 𝑅 +𝑅
𝑅
Green ratio vegetation index GRVI Sripada et al. (2006)
𝑅
Burgos-Artizzu et al.
Modified excess green MEXG 1.262𝑅 − 0.884𝑅 − 0.311𝑅
(2011)
𝑅 −𝑅
Modified normalized green red difference MNGRD Bendig et al. (2015)
𝑅 +𝑅
𝑅 −𝑅
Normalized difference Red-Edge NDRE Wang et al. (2019)
𝑅 +𝑅

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Remote detection of water and nutritional status of soybeans using UAV-based images

𝑅 −𝑅
Normalized difference Red-Edge index NDREI Hassan et al. (2018)
𝑅 +𝑅
𝑅−𝑅
Normalized difference vegetation index NDVI Gitelson et al. (2005)
𝑅+𝑅
𝑅
Normalized green NG Woebbecke et al. (1995)
𝑅 +𝑅 +𝑅
𝑅 −𝑅
Normalized green red difference NGRD Hamuda et al. (2016)
𝑅 +𝑅
𝑅 −𝑅
Optimized Soil Adjusted Vegetation Index OSAVI Rondeaux et al. (1996)
𝑅 + 𝑅 + 0.16
Pigment-specific normalized difference 𝑅 −𝑅
PSND Blackburn (1998)
index 𝑅 +𝑅
Renormalized Difference Vegetation 𝑅 −𝑅
RDVI Roujean & Breon (1995)
Index (𝑅 − 𝑅 ) .
𝑅
Red-Edge chlorophyll index RECI −1 Gitelson et al. (2005)
𝑅
Red-green difference GDPR 𝑅 −𝑅 Sanjerehei (2014)
𝑅
Ratio vegetation index RVI Tucker (1979)
𝑅
1.5(𝑅 − 𝑅 )
Soil Adjusted Vegetation Index SAVI Zhong et al. (2019)
(𝑅 + 𝑅 + 0.5)
Simplified canopy chlorophyll content 𝑁𝐷𝑅𝐸
SCCCI Raper & Varco (2015)
index 𝑁𝐷𝑉𝐼
Transformed chlorophyll absorption in Nir 𝑅
TCARI 3 (𝑅 − 𝑅 ) − 0.2 𝑅 − 𝑅 Haboudane et al. (2002)
index 𝑅
TCARI- 𝑇𝐶𝐴𝑅𝐼
TCARI/OSAVI index Haboudane et al. (2002)
OSAVI 𝑂𝑆𝐴𝑉𝐼
Transformed chlorophyll absorption in the 𝑅
TCARI-RE 3 (𝑅 − 𝑅 ) − 0.2 𝑅 −𝑅 Daughtry et al. (2000)
Red-edge index 𝑅
TCARI- 𝑇𝐶𝐴𝑅𝐼
TCARI/OSAVI-RE index Daughtry et al. (2000)
OSAVI-RE 𝑂𝑆𝐴𝑉𝐼
Triangular greenness index GIT 𝑅 − (0.39𝑅 ) − (0.61𝑅 ) Hunt et al. (2011)
(0.12𝑅 ) − 𝑅
Wide dynamic range vegetation index WDRVI Gitelson (2004)
(0.12𝑅 ) + 𝑅
𝑅
Weighted difference vegetation index WDVI 𝑅 −𝑅 Clevers (1989)
𝑅
Rn: Spectral reflectance - near infrared (840 nm); Rg: Spectral reflectance - green (560 nm); RRE: Spectral reflectance - near red (717 nm); Rr:
Spectral reflectance red (668 nm) and Rb: Spectral reflectance - blue (475 nm); R'n: Spectral reflectance - near infrared (soil); R'r: Red spectral
reflectance (soil).

Gas exchange measurements were performed in the drying, the samples were processed and used for plant tissue
electromagnetic spectrum IR region, using a portable gas chemical analysis for N by the Kjeldahl method (Teixeira et
analyzer LI-COR model 6400XT (LI-COR, Lincoln, NE, al., 2017). Leaf dry biomass and N content data were used
USA), equipped with a measuring chamber and artificial to estimate leaf N accumulations per unit area (g m-2), with
lighting LI-COR model 6400-02B. The measurements were the dry biomass per area being estimated based on each
performed on the same day of the flight, using one plant per subplot stand.
subplot of the cultivar BRS-8980 at the R3 stage, between The data were subjected to the Shapiro-Wilk test
8:00 and 10:00 am, under cloudless conditions. The extracted (normality of errors) and Cochran’s t-test (homogeneity of
data provided by Open Software version 6.3 were as follows: variance). Once the basic normality criteria were met, the
A: Net CO2 assimilation rate (micromol CO2 m-2 s-1), gs: data were subjected to analysis of variance, mean comparison
stomatal conductance (mmol H2O m-2 s- 1), and E: test (Tukey’s test) at 5% probability, Pearson’s correlation (r),
transpiration rate (mmol H2O m−2 s−1). and regression between vegetation indexes and measurements
Leaf N accumulation (NF) was quantified on the of stomatal conductance (gs) and leaf N accumulation (NF).
same day of the flight in plants of the cultivar BONUS at The statistical analyses were performed using the ExpDes.pt
the R5 stage. Four plants were collected from each subplot package of the R software (Ferreira et al., 2018). The degree
and split into organs (stem, leaves, reproductive structures, of fit of the linear regression models for estimating gs and NF
and grains), washed in running and distilled water, and then was evaluated by the coefficient of determination (R2)
dried in a forced-air oven at 65 °C until reaching constant (equation 1) and standard error of the regression (SEE), which
weight for subsequent dry biomass quantification. After represent the average distance of the observed values

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Aderson S. de Andrade Junior, Silvestre P. da Silva, Ingrid S. Setúbal, et al.

concerning the line of the regression (equation 2). For this Y ̀m - means of gs and NF estimated by the regression
purpose, the Excel Real Statistics Resource Pack (version 7.6) models.
supplement (Zaiontz, 2020) was used.
∑ ( )
RESULTS AND DISCUSSION
𝑅 = (1)
∑ Irrigation depths and soil moisture
Table 3 shows the accumulated irrigation depths
∑ ( )
𝑆𝐸𝐸 = (2) (mm) for each water regime (WR) applied during the
soybean season. From the beginning of irrigation until the
Where: application of differentiated WRs (IT), accumulated
n - number of observations; irrigation depths were 125.3 and 127.1 mm for treatments
with 50 and 100% ETc, respectively. Therefore, during the
Yi - gs and NF values measured in the field; initial period, both treatments received similar irrigation
Y ì - gs and NF values estimated by the regression models, depths regardless of the soybean cultivar.

TABLE 3. Accumulated irrigation depths (mm) for each water regime applied during the soybean crop season. Teresina, PI, 2019.
WR (% ETc) S – IT IT – TT TT – TI Season
BONUS
50 % ETc 125.3 132.9 87.6 345.8
100 % ETc 127.1 252.8 85.3 465,2
BRS-8980
50 % ETc 125.3 174.6 56.1 356.0
100 % ETc 127.1 326.5 57.7 511.3
WR: water regime (% ETc); S: sowing date; IT: beginning of the application of differentiated WRs (40 DAS) (V3); TT: end of the application
of differentiated WRs (72 DAS) (R7); TI: end of irrigation application (93 – DAS for BONUS, and 103 DAS for BRS-8980) (R8).

During the application of differentiated WRs (IT- From the beginning of irrigation until the application
TT), treatments with 50% ETc received 132.9 and 174.6 of differentiated WRs (IT), the average soil moisture
mm, while those with 100% ETc had 252.8 and 326.5 mm contents in the 0.0-0.3 m depth layer were 13.0 and 14.2%
for the cultivars BONUS and BRS-8980, respectively. for treatments with 50% and 100% ETc, respectively. In the
During the IT-TT period, deficit irrigation (50% ETc) 0.3-0.6 m depth layer, the soil moisture contents averaged
corresponded to 47% of the full irrigation (100% ETc) for 8.6% for 50% ETc and 10.3% for 100% ETc (Figure 2).
both soybean cultivars. Thus, irrigation depths were
These results demonstrate that, before the application of
different between the WR evaluated. After the application
differentiated WRs, the average soil moisture in the 0.0-0.3
of differentiated WRs until the end of irrigation (TT-TI),
treatments with 50% ETc received 87.6 and 56.1 mm, while m depth layer for both WRs was close to and above the
those with 100% ETc had 85.3 and 57.7 mm for the critical level for soybeans (12.5%), thus favoring the full
cultivars BONUS and BRS-8980, respectively (Table 3). development of the crop.
Throughout the crop season, for both soybean cultivars, Throughout the application of differentiated WRs
treatments with 50% ETc received irrigation depths of (IT-TT), the average soil moisture in the 0.0-0.3 m depth
345.8 mm for the cultivar BONUS, and 356 mm for the layer was 9.9 and 14.7% for treatments with 50 and 100%
cultivar BRS-8980. Under full irrigation (100% ETc), 465.2 ETc, respectively; in the 0.3-0.6 m depth layer, these
mm were applied for the cultivar BONUS, and 511.3 mm contents were 7.7% for 50% ETc and 12.7% for 100% ETc.
for the cultivar BRS-8980 (Table 3). These irrigation depth From the beginning of irrigation until the flight date (62
differences may be related to each cultivar maturation DAS; at R5 stage for BONUS and R3 for BRS-8980), the
group, i.e., BONUS (7.9) and BRS-8989 (8.9). In this sense, average soil moisture contents in the 0.0-0.3 m depth layer
some studies have pointed out that, depending on soil were 10.0% and 13.2% for treatments with 50% and 100%
conditions, climate, sowing date, and cultivars, soybeans
ETc, respectively, while in the 0.3-0.6 m depth layer these
may require total irrigation depths from 450 to 850 mm
contents were 7.6% for 50% ETc and 12.3% for 100% ETc
during the crop season to achieve maximum grain yields
(Allen et al., 1998). (Figure 2).

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Remote detection of water and nutritional status of soybeans using UAV-based images

FC: field capacity; CM: critical moisture; PWP: permanent wilting point; TI: beginning of the application of differentiated WR (40 DAS)
(V3); TT: end of the application of differentiated WR (72 DAS) (R7); IT: end of irrigation application (93 DAS) (R8); Flight: flight date (62
DAS; at R5 stage for BONUS and R3 for BRS-8980).
FIGURE 2. Soil moisture changes during the soybean crop season in the 0.0-0.3 and 0.3-0.6 m depth layers in response to the
applied water regimes (WR). Teresina, PI, 2019.

Our results show that, in both depth layers (0.0-0.3 Vegetation indexes and gas exchange
and 0.3-0.6 m), full irrigation kept soil moisture above Among the gas-exchange-related parameters, for
critical levels, allowing proper soybean development and the cultivar BRS-8980, only stomatal conductance (gs) had
production. Conversely, deficit irrigation promoted soil significant changes (p<0.01) in response to the WRs
moisture levels below the critical and above the permanent applied. However, no significant effect was observed due to
wilting point during the evaluated period, limiting soybean N supplementation levels (NS) or WR*NS interaction
(Table 4). Moreover, neither internal CO2 concentrations
development and grain yields.
nor transpiration showed responses to those parameters.
TABLE 4. F-test for stomatal conductance (gs), leaf nitrogen content (NF), and vegetation indexes (VIs) in response to water
regimes (WR) and nitrogen supplementation levels (NS) for the soybean cultivars BRS-8980 and BONUS. Teresina, PI, 2019.
BRS-8980 BONUS BRS-8980 BONUS
VI VI
WR NS WR*NS WR NS WR*NS WR NS WR*NS WR NS WR*NS
gs ** ns ns OSAVI *** ns ns ** ns ns
NF * * ns PSND ** ns ns ** * ns
CI-RED *** ns ns *** ns ns RDVI *** ns ns *** ns ns
CVI *** *** ns *** ns ns RECI *** ns ns *** ns ns
EVI *** ns ns *** ns ns RED ns ns ns ** * ns
EVI2 *** ns ns *** ns ns RED-EDGE * ns ns ** * ns
EXGR * *** ns * ** ns GDPR * ns ns ns ns ns
CI *** ** ns *** ns ns RVI *** ns ns *** ns ns
GLI ** *** ns ns ** ns SAVI *** ns ns *** ns ns
GNDVI *** * * ** ns ns SCCCI *** ns ns *** ns ns
GREEN * ** ns ** ns * ICART *** ns ns *** ns ns
GRVI *** ** ns *** ns ns TCARI-OSAVI *** ns ns *** ns ns
MEXG ** *** ns ** ns ns TCARI-OSAVI-RE ns * ns ** * *
MNGRD ns *** ns ** ** ns TCARI-RE ns * ns ** * *
NDRE *** * ns *** ns ns GIT ** *** ns ** ns ns
NRDEI ** * ns ** ns ns WDRVI *** ns ns ** ns *
NDVI *** ns ns ** ns ns WDRVI-1 *** ns ns *** ns *
NG ** *** ns ns ** ns WDRVI-2 *** ns ns ** ns ns
NGRD ns *** ns ** ** ns WDVI ns ns ns ns ns *
NIR *** ns ns *** ns ns
WR: ETc-based water regime (50-ETc and 100-ETc); NS: nitrogen supplementation levels (N0 and N1). Significance levels by the F-test:
***: p <0.001; **: p <0.01; *: p <0.05; ns: non-significant.

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Aderson S. de Andrade Junior, Silvestre P. da Silva, Ingrid S. Setúbal, et al.

For the cultivar BRS-8980, except for NGRD, treatments under deficient irrigation (487.6 mmol H2O m-2
TCARI-OSAVI-RE, TCARI-RE, and WDVI IVs, all the s-1) (Figure 3). Machado Junior et al. (2017) and Silva et al.
other VIs responded to the applied WRs. On the other hand, (2020) also observed gs reductions in soybeans under soil
for the cultivar BONUS, only GLI, NG, RGD, and WDVI water restriction. Stomatal conductance was the highest
did not respond to this factor. The VIs with a significant F- when solar radiation was high and leaf water potential had
test had the potential to detect soybean water status;
not yet reached minimum values to induce stomatal closure.
however, the promising VIs were those showing the highest
correlations with stomatal conductance measurements Under soil water restriction, soybeans tend to reduce
performed in the field. stomatal conductance, as a strategy to avoid water losses to
Stomatal conductance (gs) in treatments under full the atmosphere, but reducing photosynthetic activity and
irrigation (690.8 mmol H2O m-2 s-1) was higher than that of hence grain yields (Gorthi et al., 2019).

FIGURE 3. Stomatal conductance (cultivar BRS-8980) in response to the water regimes (WR) applied to soybeans. Teresina,
PI, 2019.

Chavarria et al. (2015) observed that soil water photosynthetic rates. Furthermore, due to higher leaf
potentials equal to or below -0.026 MPa cause significant activity and continuous N supply, N2 fixation slows leaf
reductions in the photosynthetic activity of soybeans, of the senescence and increases grain filling in soybean plants
cultivar 'BMX Apolo RR', due to lower gs under water (Kaschuk et al., 2010).
deficiency in the soil. The authors obtained gs equal to The parameter gs showed a significant correlation
741.0 mmol H2O m-2 s-1 under adequate water availability with several VIs. As the VIs with r≥0.6 are considered
conditions in the soil (-0.004 MPa), while under soil water promising (Yue et al., 2020), the six best VIs to detect water
restriction (-0.026 MPa) it decreased to 426.5 mmol H2O m- status were: NIR (r = 0.6779; p<0.001), EVI (r = 0.6741; p
2 -1
s , which is very close to our values. Karaca et al. (2018) <0.01), SAVI (r = 0.6723; p <0.01), RDVI (r = 0.6713; p
obtained mean values of gs for two soybean cultivars equal <0.01), OSAVI (r = 0.6611; p <0.01), and NDRE (r =
to 574.5 mmol H2O m-2 s-1 under full irrigation and 251.5
0.6294; p <0.01) (Figure 4). A few studies have indicated
mmol H2O m-2 s-1 under water deficit conditions in the soil.
that VIs using spectral bands in the NIR are the most
Given the importance of biological N fixation for
soybeans, one should note that this process can be suitable to detect water status in crops grown in soils under
compromised by water restriction (Chavarria et al., 2015). water stress conditions (Elsayed et al., 2015). In our study,
Under conditions of water stress, there is a reduction in EVI, SAVI, RDVI, OSAVI, and NDRE fit the condition
biological nitrogen fixation and a consequent decrease in established by Elsayed et al. (2015).

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Remote detection of water and nutritional status of soybeans using UAV-based images

Significance levels by the t-test: ***: p<0.001; **: p<0.01; *: p<0.05; ns: non-significant.
FIGURE 4. Pearson’s correlation between the evaluated vegetation indexes (VI) and leaf stomatal conductance (gs) for the
cultivar BRS-8980. Teresina, PI, Brazil, 2019.

Soybean Leaf water potential (Ψf) was correlated index, mainly at the reproductive stage, with potential for
with the spectral indexes evaluated by Wijewardana et al. phenotyping and as a water deficit tolerance indicator.
(2019b). The indexes NDVI (r = 0.905), RNDVI (r = 0.905),
Vegetation indexes and leaf nitrogen accumulation
NWI (r = 0.866), NWI4 (r = 0.843), and NWI5 (r = 0.742)
increased linearly with increasing leaf Ψf values. In our Leaf N accumulations (NF) in the cultivar BONUS
study, this parameter showed a positive linear correlation were significantly affected (p <0.05) by the WRs and N
with gs in soybean leaves (y = 0.94 + 0.60x, R2 = 0.6). supplementation (NS) levels (Table 4). For the cultivar
NDVI had a higher correlation (r = 0.905) with leaf water BRS-8980, the indexes CVI, EXGR, GLI, MEXG,
potential than did the other VIs. Overall, NDVI is the index MNGRD, NG, NGRD, and TGI responded to the N
that best indicates soil cover by plant canopy (Zhao et al. supplementation (NS) levels applied to the soil (p<0.001),
2007). Soil water stress reduces chlorophyll and other while for the cultivar BONUS the indexes EXGR, GLI,
photosynthetic pigments, thus reducing the biomass and MNGRD, NG, and NGRD stood out (p<0.01) (Table 4).
height of soybean plants, hence resulting in low NDVI These Vis, therefore, have the potential for N detection in
values (Crusiol et al., 2017). soybeans; however, the promising VIs will be those with the
We observed that trend since NDVI and gs best correlations with the NF measurements performed in
correlation reached only r = 0.576 (p <0.01). However, the the field.
indexes EVI, SAVI, RDVI, OSAVI, and NDRE, which use Full irrigation promoted higher leaf N accumulations
spectral bands in the NIR region, stood out in detecting (6.4 g N m-2) than did deficit irrigation (4.3 g N m-2) (Figure
soybean water status. This is because they allowed gs 6). Nitrogen supplementation showed higher leaf N
estimates with R2 ranging from 0.462 (NIR) at 0.4506 accumulation (5.5 g m-2) compared to the absence of N
(RDVI) and SSE from 108.1 (NIR) at 109.2 mmol H2O m-2 application (5.2 g N m-2) (Figure 6). The lowest leaf N
s-1 (RDVI) (Figure 5). Wijewardana et al. (2019b) obtained accumulation (4.3 g N m-2) was observed under deficit
a positive linear correlation between Ψf and NDVI, using irrigation conditions (Figure 6). According to Chavarria et
the ratio y = 0.9495+0.08636x (y: NDVI ex: Ψf, in MPa) al. (2015), biological nitrogen fixation by soybeans may be
and R2 = 0.82; therefore, NDVI can be used as a promising compromised by soil water restriction, decreasing
VI to detect soybean water status. Crusiol et al. (2017) also photosynthetic rates and hence final grain yields (Basal &
concluded that NDVI can be used as a soybean water status Szabó, 2020).

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Aderson S. de Andrade Junior, Silvestre P. da Silva, Ingrid S. Setúbal, et al.

FIGURE 5. Regression between promising vegetation indexes and leaf stomatal conductance for the soybean cultivar BRS-
8980. Teresina, PI, Brazil, 2019. Significance levels by t-test: ***: p<0.001; **: p<0.01; *: p<0.05; ns: non-significant.

FIGURE 6. Leaf nitrogen accumulations in the soybean cultivar BONUS in response to the water regimes (WR) and nitrogen
supplementation (NS) applied to the soil. Teresina, PI, Brazil, 2019. Means followed by the same letter do not differ from each
other by the F-test (p<0.05). Lowercase (WR) and uppercase (NS) letters.

In a study performed in Piracicaba city - SP (Brazil) the cultivars had different cycles, maturation groups, and
with the soybean cultivar RK7518 IPRO (indeterminate plant population stands.
growth habit, average growth cycle, and maturation group Leaf N accumulation (NF) had significant
7.5), Zambon (2020) observed that leaf N accumulations correlations with several VIs evaluated in our study.
reached maximum levels at the first phenological stages Considering as promising the VIs with r≥0.6 (Yue et al.,
(64.2 g N kg-1) and then had gradual reduction until the R6 2020), the six best ones for detecting leaf N accumulations
stage (23.1 g N kg-1). These authors observed a leaf N were: CVI (r = 0.7266; p <0.001), NIR (r = 0.7065; p
<0.001), RECI (r = 0.6912; p <0.001), GCI (r = 0.6869; p
concentration of 27.3 g N kg-1 dry leaf biomass at the R5.2
<0.001), GRVI (r = 0.6869, p <0.001), and SCCCI (r =
stage (85 days after soybean emergence); as dry leaf 0.6795; p <0.001) (Figure 7). Moreover, for plant N
biomass was 444.1 g m-2, leaf N accumulation was 12.12 g contents, the same indexes stood out: CVI (r = 0.7601; p
N m-2. This N accumulation was higher than that observed <0.001), GIT (r = -0.6923; p <0.001), SCCCI (r = 0.6803; p
in our study under full irrigation (6.4 g N m-2). This may be <0.001), RECI (r = 0.6749; p <0.001), GCI (r = 0.6733; p
due to leaf dry biomass differences between both studies, as <0.001), and GRVI (r = 0.6733; p <0.001) (Figure 7).

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Remote detection of water and nutritional status of soybeans using UAV-based images

Significance levels by the t-test: ***: p <0.001; **: p <0.01; *: p <0.05; ns: non-significant.
FIGURE 7. Pearson’s correlation between vegetation indexes and leaf nitrogen accumulations for the soybean cultivar BONUS.
Teresina, PI, Brazil, 2019.

Yue et al. (2020) evaluated soybean leaf chlorophyll to 0.7475 (p <0.001) and SSE from 0.500 g m-2 to 0.618 g
contents using VIs from multispectral images and found m-2 (Figure 8). Such a superior performance of SCCCI in
that the best ones in terms of Pearson’s correlation (r) were: predicting leaf N contents has already been reported for
TCARI/OSAVI-RE (r = 0.95; p <0.01), PSND (r = 0.88; p other crops. For instance, among the numerous VIs
<0.01), and NDRE2 (r = 0.85; p <0.01). These authors evaluated by Raper & Varco (2015), SCCCI had the best
concluded that soybean leaf chlorophyll contents are correlation with leaf N contents in cotton (r = 0.787). As in
directly related to leaf N contents and emphasized that VI our study, these authors found an increasing linear
performance in detecting chlorophyll contents depends on regression between SCCCI and leaf N contents (R2 = 0.62).
soybean leaf area indexes. Therefore, the ratio between VI For wheat plants, Cammarano et al. (2011) also concluded
and chlorophyll content must be defined for different that SCCCI has potential for leaf N content estimations (y
soybean phenological stages. = 0.94x + 0.15; R2 = 0.97; RMSE = 0.2 g N m-2) and
In our study, the indexes SCCCI, RECI, GRVI, CVI, suggested future studies to validate its applicability under
TCARI-OSAVI, and TCARI promoted the best leaf N different production environments, sowing dates, and soil
content estimates, with R2 ranging from 0.8347 (p <0.001) water conditions.

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Aderson S. de Andrade Junior, Silvestre P. da Silva, Ingrid S. Setúbal, et al.

Significance levels by the t-test: ***: p <0.001; **: p <0.01; *: p <0.05; ns: non-significant.
FIGURE 8. Linear regression between promising vegetation indexes and leaf nitrogen contents for the soybean cultivar
BONUS. Teresina, PI, Brazil, 2019.

In a study with corn, Ciganda et al. (2009) found that Bendig J, Yu K, Aasen H, Bolten A, Bennertz S, Broscheit
RECI was a promising index to estimate leaf chlorophyll J, Gnyp ML, Bareth G (2015) Combining UAV-based
contents and reported a linear regression, with R2 = 0.9429 plant height from crop surface models, visible, and near-
and SSE = 50.9 mg N m -2 (y = 37.904+1353.7x). These infrared vegetation indices for biomass monitoring in
authors highlighted a high linear correlation between barley. International Journal of Applied Earth
Observations 39:79-87. DOI:
model-estimated and field-observed chlorophyll contents
https://doi.org/10.1016/j.jag.2015.02.012
(R2 = 0.9761; RMSE = 37.5 mg N m-2); thus, RECI has great
potential for estimating leaf chlorophyll contents in Bian J, Zhang Z, Chen J, Chen H, Cui C, Li X, Chen S, Fu
corn plants. Q (2019) Simplified evaluation of cotton water stress
using high resolution unmanned aerial vehicle thermal
CONCLUSIONS imagery. Remote Sensing 11:267-274. DOI:
https://doi.org/10.3390/rs11030267
The near-infrared spectral band and the vegetation
Blackburn, GA (1998) Quantifying chlorophylls and
indexes EVI, SAVI, and RDVI are promising for detecting carotenoids at leaf and canopy scales: An evaluation of
soybean water status, while the indexes SCCCI, RECI, some hyperspectral approaches. Remote Sensing of
GRVI, and CVI are promising for estimating soybean Environment 66:273-285. DOI:
nutritional status in terms of nitrogen contents. https://doi.org/10.1016/S0034-4257(98)00059-5
Burgos-Artizzu XP, Ribeiro A, Guijarro M, Pajares G
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