International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340

Contents lists available at ScienceDirect

International Journal of Applied Earth

Observations and Geoinformation
journal homepage: www.elsevier.com/locate/jag

Retrieval of betalain contents based on the coupling of radiative transfer

model and SVM model
Rukeya Sawut a, b, Ying Li a, b, *, Yu Liu c, Nijat Kasim d, Umut Hasan e, f, Wei Tao c
a
Navigation College, Dalian Maritime University, Dalian 116026, China
b
Environmental Information Institute, Dalian Maritime University, Dalian 116026, China
c
College of Environmental Science and Engineering, Dalian Maritime University, Dalian 116026, China
d
College of Biology and Geography, Yili Normal University, Yining 835000, China
e
Institute of Applied Remote Sensing and Information Technology, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, Zhejiang 310058,
China
f
Key Laboratory of Agricultural Remote Sensing and Information Systems, Zhejiang University, Hangzhou, Zhejiang, 310058, China

A R T I C L E I N F O A B S T R A C T

Keywords: Betalain (Bt) is as a class of edible natural pigments and important biochemical aparmeter can explain the
Betalain contents physiological response and the resistance of plants caused by different environmental stress factors. Hyper­
Radiative transfer model spectral spectroscopy has been widely used to estimate plant pigments contents accurately and non-destructively.
SVM model
However, there is very little research about hyperspectral remote sensing estimation and inversion of betalain
Spectral indices
contents. The algorithm of Bt content inversion with viable universality is the key to improving the practicality of
Remote sensing inversion
quantitative remote sensing. Therefore, in this study, based on the radioactive transfer mechanism and SVM
model, the optical characteristics of Bt and other factors of Suaeda salsa are analyzed, and a coupling model
(PROSAIL + SVM) of simulated canopy reflectivity and factor contents is established. The model was then
applied to the remote sensing inversion. Results demonstrated that Bt content was sensitive to the spectral range
between 460 and 592 nm, particularly between 530 and 550 nm where the sensitivity index reached 0.7.
Optimized indices; NDSI473nm,475nm, RSI473nm,475nm and NDPI473nm,475nm, calculated by simulated spectral
reflectance had a significant correlation with Bt content (R= ±0.80, p < 0.001). Moreover, simulated Sentinel-2A
reflectance of the Blue (B2) and Green (B3) bands showed sensitivity of 66% and 68%, respectively. Spectral
indices NDPI b2, b3, NDSI b2, b3, RSIb2, b3 showed correlation of ± 0.71. The PROSAIL + SVM model developed
from simulated hyperspectral reflectance, estimated Bt content with high R2 (0.82), indicating that the precision
of the model was higher and the universality was stronger. A model composed of optimized indices (NDSI473nm,
− 2
475nm, RSI473nm, 475nm and NDPI473nm, 475nm) showed promising estimation ability with low RMSE (0.39 μg⋅cm )
with R2 = 0.78 and RPD = 1.99. When the PROSAIL + SVM model was extended to multispectral images
(Sentinel-2A), the model estimated the Bt content at moderate to good levels (R2 = 0.68). The results indicated
that optimized hyperspectral and multispectral NDPI, NDSI, RSI have significant correlation with betalain
content of S. salsa, suggesting these indices might be used to quantify Bt content with high accuracy, thereby
alleviating the ill-posed inverse problem and improving sensitivity. Not only would this enhance the application
of quantitative remote sensing technology in betalain research, but the results also pose positive application for
precision agriculture in detecting Bt pigments in crops, as a surrogate for evaluating the health condition of
crops.

1. Introduction
Plant leaf pigment, as one of the most important biochemical pa­
rameters in crops, plays a crucial role in the evaluation of physiological
and ecological growth conditions (Feret et al., 2011; Rahimzadeh-
Bajgiran et al., 2012). Pigments are mainly divided into photosyn­
thetic pigments (chlorophyll and carotenoids) and non-photosynthetic
pigments (anthocyanidins, betalains, etc.). Betalains are a class of
tyrosine-derived non-photosynthetic pigments, red (betacyanins) or
yellow (betaxanthins) in color, and are present in plants of the order

* Corresponding author at: Navigation College, Dalian Maritime University, Dalian 116026, China.
E-mail address: yldmu@126.com (Y. Li).

https://doi.org/10.1016/j.jag.2021.102340
Received 1 October 2020; Received in revised form 3 April 2021; Accepted 6 April 2021
Available online 22 April 2021
0303-2434/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
R. Sawut et al.
Carophyllales. Insects are attracted by the color and aid in pollination,
while birds and other foragers transport seeds to different places. Thus,
the betalains contribute significantly to the propagation and spread of
the plants (Nemzer et al., 2011). In addition, betalains play an important
role in plants’ protection mechanisms, existing in the root system of
plants. It is suggested that betalains work for plants’ resistance to soil-
borne diseases, flooding, drought, and other biotic and abiotic stresses
(Zhang et al., 2015). The dynamics of betalain’s concentration plays a
crucial role in explaining the physiological response and resistance of
plants caused by environmental stress or seasonal fluctuations (Delga­
dovargas et al., 2000; Tanaka et al., 2008). Most plants containing
betalain grow well in drought or saline soils. It is proposed that there is a
close correlation between its vitality and betalain (Strack et al., 2003;
Grewal et al., 2017). Thus, a study on betalain content of vegetation is
necessary to further illustrate the growth status and as a possible indi­
cator to monitor the changeable environment.
Studies indicated that plant leaf pigments have obvious spectral
characteristics with unique absorption bands in the visible spectrum
(400–800 nm) (Sims and Gamon, 2002), occupying the high-energy
spectrum of sunlight which reaches most areas of the ground
(200–1100 mn) (Kiang et al., 2007). The maximum absorption wave­
length in betalains occurs around 538 nm (Wang et al., 2007). Due to the
information-rich hyperspectral data that is available, studies have been
carried out on estimation and detection of some pigments such as
chlorophyll and cartenoid in plant leaves on the basis of its spectral
characteristics (Gitelson et al., 2006; Wang et al., 2016; Sun et al., 2018).
However, there are few studies on the estimation and inversion of
betalain content from hyperspectral data. Therefore estimating the
betalain content of Suaeda salsa via hyperspectral data has certain
practical significance.
Remote sensing is convenient, effective, and non-destructive to
detect the nature of vegetation (Lu et al., 2018; Casas et al., 2014; Xiao
et al., 2014). Furthermore, hyperspectral remote sensing techniques
enable the realization of narrow spectral band’s information and higher
accuracy of estimation on vegetation biochemical parameters (Wang
et al., 2016). At present, methods for estimating vegetation pigments
content through remote sensing data are basically divided into two
categories: empirical and semi-empirical statistical methods and optical
physical model methods (Wang et al., 2015; Wu et al., 2012). Though
the empirical model method is relatively mature and widely used (Wu
et al., 2012; Luo et al., 2018), it is limited by the saturation effect.
Moreover, the dependence of acquired experience with the scene and
the sensor, limits its versatility (Vamvakoulas et al., 2020). The identi­
fication of exact sensitive spectral bands is difficult because absorption
peaks from multiple biological compounds tend to overlap, such as
chlorophyll and carotenoid (Wang et al., 2016). In addition, the radia­
tive transfer model is one of the most widely used optical physical
methods (Jing et al., 2012), although it is suitable for horizontal uniform
vegetation or turbid media (Pan et al., 2013). The PROSPECT5 model
proposed by Feret (2011) divided photosynthetic pigments into chlo­
rophyll and carotenoids, for exploration of photosynthetic properties of
leaves. The calculation of a new refractive index and setting of more
reasonable leaf parameters makes simulated leaf reflectance more ac­
curate (Wang et al., 2016; Yang et al., 2010; Zeng et al., 2016; Li and
Wang, 2013; Xu et al., 2019). Compared to other methods, the radiative
transfer model contains precise physical information, with flexibility in
its variable parameterisation. Furthermore, simulated data from the
model has become the main data source for performing inversion of
vegetation biochemical parameters (Wang et al., 2016). The PROSPECT
+ SAIL (PROSAIL) model was developed (Baret et al., 1992) for
dimensional reduction in inversion problems and evaluation of
biochemical parameters of the canopy. At present, PROSAIL is
commonly used for estimation of chlorophyll content, leaf area index
(LAI), and other biochemical parameters at the canopy level (Berger
et al., 2018; Duan et al., 2014; Si et al., 2012). Meanwhile, sustained
reforming in the spectral resolution of optical sensors have provided
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International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340
new chances for detection and quantification of individual lobar pig­
ments at large-scales (Verrelst et al., 2015). Due to the complexity of the
radiative transfer model, some studies have proposed a new method of
coupling radiative transfer models with help of multilinear regression
models (Wang et al., 2015), support vector machine (SVM) models
(Boser et al., 1992; Lü, 2012), and random forest (RF) models (Ho, 1995;
Naomi et al., 2018), and obtained high inversion accuracy. Studies
coupling canopy radiative transfer models and machine learning algo­
rithms attempt to understand the scale-up strategy of the relationship
between canopy optical index and vegetation physiological parameter
content (Prasad et al., 2012). These methods improve the spectral index
of background reflection that is not sensitive to certain factors such as
canopy structure, lighting geometry, to estimate the contribution of leaf
physiological parameters from the canopy reflectance (Thenkabail et al.,
2014; Lü, 2012).
As an important physiological component of vegetation leaves,
betalain pigments improve the ability of plants to resist freezing and
drought stress, and has a crucial role in the adaptation of vegetation to
the ecological environment. The dynamic information of Bt content
shows the physiological responses of plants caused by different envi­
ronmental stress factors or seasonal fluctuations(Wang et al., 2017).
Therefore, in this study, by further quantifying the influence factors of
the optical properties of the plant canopy in the characteristic band of
the Bt spectrum, a new canopy Bt radiative transfer model was con­
structed. The Suaeda salsa plant which is rich in Bt pigment, was selected
as the study vegetation. The PROSAIL model, optimized spectral index
and the SVM model were applied to estimate Bt content and the remote
sensing inversion of Bt content on various spectral scales. This research,
on the one hand, adds to the comparatively little research on Bt content
in the hyperspectral monitoring of vegetation natural pigment content,
while on the other hand, it has certain scientific significance in spatio­
temporal monitoring of changes in physiological parameters of the
degraded Suaeda salsa, due to the influence of human activities and
natural factors, such as the succession of vegetation communities in the
coastal wetland area.
2. Materials and methods
2.1. Basic idea
The flow chart of the mean idea of the study is shown in Fig. 1. First
of all, we selected the study sites and collected the all necessary datasets,
such as spectral data (hyperspectral data and Sentinel-2A) and vegeta­
tion parameters (batalain contents, leaf area, chlorophyll contents, leaf
water contents and weight of dry matter), respectively (detailed data
collection procedure and processing, see Section 2.3). Then we simu­
lated S. salsa canopy reflectance based on the PROSAIL model and
recalibrated the model parameters using by sensitivity analysis and
fitness degree of spectral reflectance (see Section2.4). On the three step
based on the sensitivity results selected the sensitive bands of batalain
contents and calculated the optimized hyperspectral indices (RSI, NDSI,
and NDPI) by using MATLAB (see Section 2.6). On the fourth step,
converted the simulated canopy reflectance to the Sentinel-2A reflec­
tance. At the end, constructed the SVM model at the different spectral
scale and obtained inversion of map batalain contents. all steps was
explained in detail from Sections 2.3–2.8.
2.2. Study area
“Red Beach” is located in Panjing City, Liaoning Province (Fig. 2(a)),
China, it situated on the north side of Liaodong Bay of Bohai Sea
(N40◦ 39′ ~ 41◦ 27′ , E121◦ 23′ ~122◦ 29′ ) (Fig. 2(b)) the total area oc­
cupies approximately 12.8 × 104 ha. The climate is a temperate semi­
humid monsoon climate, the average annual rainfall is 650 mm.In this
study, the authors selected the Suaeda salsa (S. salsa) as the betalain
source (Fig. 2(c, d)). Recent studies (Wang et al., 2006; Wu et al., 2008;
R. Sawut et al.
Fig. 1. Flow chart of the study.
Jain and Gould, 2015) have indicated that the red pigment in S. salsa
leaves can also be identified as betalain; In comparison to other plants’
sources, such saline-alkaline plant species contains very little sugar,
which could simplify the pigment extraction process in a great extent
(Wang et al., 2006).
2.3. Datasets
2.3.1. Experimental data
2.3.1.1. Collection of spectral data. The spectral reflectance of S. salsa
leaves was measured with the assistance of ASD FieldSpec®3 portable
spectrometer (Analytical Spectral Device, USA) based on a setted
wavelength range of 350 ~ 2500 nm. The S. salsa leaves spectra were
measured under sunny weather condition for the sky was clear enough
to conduct observation and such weather is suitable for the collection of
field data (10:00–12:00). The detection height reaches to approximately
30 cm above the plant, and performed whiteboard calibration before
each spectrum measurement, repeat the measurement 5 times, and take
the average value of the spectrum curve by using View SpecPro V6.0
software. Due to the certain factors such as strong atmospheric ab­
sorption (1349 ~ 1451 nm, 1795 ~ 2010 nm and 2350–2400 nm), in­
fluence of water vapor, and other factors, the data of the field spectral
measurement data observed from the 400 ~ 1349 nm, 1451 ~ 1795 nm,
and 2010 ~ 2350 nm band ranges were exclusively used for the study of
the spectral characteristics of the betalain.
2.3.1.2. Ground biophysical measurements. A random set of 84 sample
plots, applied using a sampling frame (area of 1 m × 1 m) was estab­
lished at theRed Beach. Leaf samples of Suaeda salsa were arbitrarily
gathered from 21 sampling plots per month (from June to September
2017). In addition, shoot cuttings were also collected. Vegetative
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International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340
samples were placed in Ziploc bags and then put in an icebox for
transport to the laboratory at the College of Environmental Science and
Engineering, Dalian Maritime University, for further processing of
samples, including chlorophyll content, leaf moisture content, leaf area
index (LAI), and the weight of dry matter. These parameters were
measured on the basis of the traditional experimental methods (Zhu
et al., 2014; Lü, 2012) as follows:
LAI: The leaf area index of crops at the sampling point was measured
by digital camera and Adobe Photoshop software (San Jose, CA, USA). A
piece of graph paper with a known area (50 cm2) was fixed to a hard
board as a background grid for photo collection (Lü, 2012). The S. salsa
leaves were spread on the background bottom plate and flattened with a
transparent plastic cover to ensure the leaves were completely flat. A
digital camera was used to photograph the S. salsa leaves, and Photo­
shop used to extract the leaf edges, thresholded, and the number of
pixels counted so that the LAI was calculated.
Bt extraction: For the measurement of total betalain (Bt) content,
several methods exist. In this study betalain extraction was based on the
experimental method of Jain and Gould, 2015. The plants of S. salsa
were washed with distilled water, the aerial parts sectioned, dried and
chopped. Nine samples of 0.50 g were weighed and dissolved in 60 ml
water, 50% ethanol, absolute ethanol, petroleum ether, ether, chloro­
form, glacial acetic acid, acetone, and methanol, respectively. The
samples were immersed left for 50 min and then centrifuged at 10,000 g
for 10 min. The supernatant was transferred into a colorimetric tube.
The color of the supernatant was observed and the extraction solvent
was preliminarily determined (Jain and Gould, 2015; Sawicki and
Wiczkowski, 2018;Wu et al., 2008).
Chlorophyll extraction: Chlorophyll was extracted via acetone
extraction. Ground leaves were put into a 50 ml centrifuge tube, 25 ml
(80%) acetone solution added, and centrifuge at 1000 rpm for 3 min.
The concentration of chlorophyll was determined by monitoring the
R. Sawut et al. International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340

Fig. 2. The geographic location of the study area.

absorbance at 645 nm and 663 nm. According to the formula (1, 2) as to obtain the surface reflectance (Hedley et al., 2018; Zoffoli et al.,
reported by Zhu et al.(2014). 2020). The image was processed using the Sentinel Application Platform
(SNAP). For atmospheric correction we used the Sen2cor algorithm; the
Cab = Cab × Vt × n/FW 1 × 1000 (1)
core of the algorithm is the atmospheric radiation transmission model -
libRadtran (Sudmanns et al., 2019). During the atmospheric correction,
Cab = Cab × FW 1 /A1 × 1000 (2)
the latitude and longitude data of the pure pixel Suaeda salsa samples
Leaf water content: The S. salsa leaves were cut into pieces and put were converted into SHP files, and imported into ENVI5.4 (Harris
into a weighing bottle for measuring the leaf weight (accuracy reached Geospatial Solutions, Inc., Broomfield, CO, USA), where the plot loca­
± 1 mg). Leaves were dried in a drying oven at 105 ◦ C for 3 h. Leaf tion was identified on the image and the correction carried out.
moisture content was calculated on the oven-dry basis (Zhu et al., 2014).
FW − DW 2.4. PROSPECT + SAIL model
EWT = × 100% (3)
A1
The PROSAIL model uses the optical properties of the leaf reflectivity
Dry matter content (Dm): Dm was calculated as the total amount of
and leaf transmittance, output by the PROSPECT model, as the input of
organic matter (dry weight) of crop per unit area per unit time (Lü et al.,
the SAIL model to simulate the canopy reflection in the entire spectral
2012).
direction (Katja et al., 2018). The PROSAIL model parameters were
DW placed in Table 1, and the model formula is as follows (Zhang et al.,
Cm (g/cm2 ) = × 100% (4)
A1 2017).

where FW and DW is dry and fresh weight of leaves, A1 leaf area, Vt is (ρ1 , τ1 ) = PROSPECT(N, Cab , Ccar , Canth , Cm , Cw ) (5)
diluent volume, n is number of leaves.
pc = 4SAIL(LAI, ρ1 , τ1 , H, Psoil , θv , θs , θz ) (6)
2.3.2. Remote sensing data
where ρ1 is leaf reflectivity,τ1 is leaf transmittance, the full name and
The Sentinel-2A multispectral image (June 31, 2017) of Panjing City
obbreviations of the other parameters were placed in Table 1.
was obtained from the European Space Agency (ESA) data portal (htt
Previous studies have indicated that the betalain and anthocyanidins
p://www.esa.int/ESA), selecting cloud- and shadow-free images, so
were mutually exclusive, as these pigments have not been observed in
that only atmospheric correction of the downloaded data was performed
plant tissue at the same time (Wu et al., 2008; Wang et al., 2006). Thus

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R. Sawut et al. International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340

Table 1 NDSI (simple normalized difference spectral index), and NDPI

Parameters in the PROSAIL model used in the sensitivity analysis (Zhang et al., (normalized polarization index). To improve the performance of the
2017). existing two-band spectral indices (Hasituya et al., 2020), the RSI, NDSI,
Model Parameter Symbol Value of range Unit and NDPI spectral indices were optimized by combining all possible two
PROSPECT Leaf structure N 1–2.5 –
wavelengths of simulated canopy hyperspectral reflectance (Rodrigues
Chlorophyll contents Cab 10–120 μg⋅cm− 2 et al., 2018).
2
Anthocyanin contents Canth 0–12 μg⋅cm−
Leaf water contents Cw 0.001–0.0014 μg⋅cm− 2 RSI = Ri /Rj (8)
2
Dry matter contents Cm 0.001–0.025 μg⋅cm−
4SAIL Leaf area index LAI 0–8 m2/m2 NDSI = (Ri − Rj )/(Ri + Rj ) (9)
Hot parameter Hspot 0.5/LAI –
Soil moisture ratio Psoil 0–1 – NDPI = (Ri + Rj ) × Rj (10)
View angle θv 0 Degree/◦
Solar zenith angle θs 27 Degree/ ◦
where R is the spectral reflectance value, i nm and j nm are wavelengths
Relative azimuth angle θz 0 Degree/◦ (nm).

in this study the effects of anthocyanin were not considered (Table2).
However, recalibration was performed according to the following three
steps: (1) simulation of canopy reflectance based on the measured pa­
rameters (chlorophyll content, betalain contents, LAI, leaf moisture
content, and leaf dry matter content; (2) other unmeasured parameters
(Hot parameter, leaf structure, soil moisture) based on the fitting degree
(RMSE value and R2) of simulated and measured canopy spectral
reflectance; and (3) other insensitive parameters following optimization
(sensitivity analysis), then determined the step value of sensitive pa­
rameters (Zhang et al., 2017). In this study, the PROSAIL model was
implemented on the Python 3.7 platform.
2.5. Sensitivity analysis
The EFAST method is one of the global sensitivity analysis (SA) (He
and Yang, 2013), combining the advantages of the Sobol method and the
Fourier amplitude sensitivity test method(Xiao et al., 2018; Iooss and
Lematre, 2014). In this study, the method was used for finding sensitive
spectral bands of Bt content and other PROSAIL parameters. For a multi-
parameter coupling model, the total sensitivity index of the parameter is
the sum of the sensitivity indexes of all orders, which can be expressed as
(Zhang et al., 2017):
STi = Si + Sij + Sijm + ⋯ + S12⋯.i⋯k
The total sensitivity index is the sum of the direct contribution rate of
the parameter and indirect contribution of interactive coupling of other
parameters, and when there is no coupling between parametersSij andSijm
both 0,STi = Si , EFAST analysis is equivalent to Local SA (He and Yang,
2013), SA was performed by Simlab software.
In this study according to the prepared datasets and Table1 randomly
sample LAI, N, Cab, Bt, Cw, Cm, Psoil, Hspot parameters 5000 times, then
used the EFAST global sensitivity analysis method to calculate the
parameter sensitivity.
2.7. SVM model
Support vector regression is an application of the support vector
machine algorithm in regression analysis. In regression-based SVM,
training data is imposed on the learning machine, from which it at­
tempts to learn the input–output relationship (Durbha et al., 2007).
Here, the radial basis function (RBF) kernel has been used as follows
(Wang et al., 2017a,b):
( ) ( )
k xi , xj = exp − φ‖xi − xj ‖2 , φ > 0 (11)
where φ is Gaussian function, xi, xj are feature vectors. This paper
applied the support vector machine algorithm in function fitting. The
establishment of a relationship between Bt content and sensitive spectral
bands as input layers served for estimation of Bt content.
2.8. Spectral scale conversion
On the basis of standardizing, collating, and collecting of the spectral
data for the summarize of typical features, the spectral measurement can
be divided into three types according to the scales of features, namely:
material spectral measurement, end element spectral measurement, and
pixel spectral measurement (Zhao et al., 2018). It is feasible to convert
(7) the spectral scales according to the research purpose of the study, but it
can be considered as inevitable to avoid overlooking information during
the process (Soudani et al., 2006). In this study, the canopy spectra of
S. salsa were simulated and converted to pixel spectra of Sentinel-2A,
and further analysed by inverting the Bt content by means of multi­
spectral remote sensing images. The Sentinel-2A reflectance is calcu­
lated as follows (Soudani et al., 2006):
∫ λ2
RSRλ RPROSAIL dλ
(12)
λ
R = 1 ∫ λ2
RSRλ dλ
λ1

R is the simulated reflectance(R-PROSAIL).λ1 and λ2 are the band

2.6. Spectral indices wavelength limits. RSR is spectral response of the sensors, in this study
we used the spectral response of Sentinel-2A (Fig. 3).
In order to quantify Bt content via a spectral index, in this study the
widely used indices were selected, such as RSI (ratio spectral index), 3. Results

3.1. Sensitivity analysis

Table 2
Ranges of the parameters of recalibrated PROSAIL model.
The Fig. 4a shows EFAST first order sensitivity coefficients and in­
Max Min Step Unit
teractions to canopy reflectance for global sensitivity analysis with the
2
Cab 16.51 10.18 1.5 μg⋅cm−
2
PROSAIL model. It illustrated that every single parameter’s first order
Bt 7.50 0.70 0.5 μg⋅cm−
sensitivity index was lower than the total order indexes (Fig. 4b). The
LAI 3.56 1.20 0.6 m2/m2
Psoil 0.35 0.1 0.15 – sum of the EFAST first-order sensitivity coefficients (Cab, Bt, Cw, LAI, N,
Cm 0.055 0.055 fixed μg⋅cm− 2 Psoil, Hspot and Cm) reached 100%, indicating that interactions of these
Cw 0.0008 0.0008 fixed μg⋅cm− 2 parameters to the canopy reflectance variability are not evident (Wang
N 2.1 2.1 fixed – et al., 2015). An obvious difference exists in sensitive spectral subsets of
Hspot 0.0003 0.0003 fixed
each parameter. Parameters like Cab, Bt, LAI, N, Psoil are sensitive within
–

5
R. Sawut et al.
Fig. 3. Spectral response curves for Sentinel-2A.
the visible range (380–780 nm) to various degrees. Cab is sensitive to the
red range (625–740 nm), with its contribution reaching 30% at
665–684 nm; Bt content sensitivity indices within the range of 460–592
nm showed high value, and in the blue (485–500 nm), cyan (485–500
nm), green (500–565 nm) and yellow (565–570 nm) ranges, contribu­
tion reached approximately 70% .
N was sensitive to orange (590–625 nm) and red (625–740 nm)
spectral ranges, with its sensitivity index reaching approximately 0.25,
particularly within the range 615–694 nm. The LAI and Psoil sensitive
spectral subsets were more complicated, displaying various contribu­
tions at different regions of visible range and near-infrared
(NIR:780–2400 nm) range. In the visible range, LAI is more sensitive
to 607–671 nm and 681–818 nm and highly sensitive to 1599–1873 nm
in the NIR range with its contribution reaching 60%. Psoil is more sen­
sitive to 400–440 nm, 485–497 nm, 943–950 nm with its sensitivity
index approaching 0.9 and the total near-infrared range contribution
rate around 60%. Cw, Cm, and Hspot are not significantly sensitive within
the visible-NIR range (400–2400 nm) with sensitive indexes lowering
than 0.10.
Based on the analysis above, it is confirmed that Bt, LAI, Psoil, Cab
contribute significantly to canopy reflectance of S. salsa, whereas Cw, N,
Cm, and Hspot sensitivity indices (around 0–0.2) suggest they are not
sensitive parameters in the overall canopy reflectance.
Each parameter varied significantly during the sensitivity analysis
while a few parameters were retained. Relative changes were studied in
Fig. 4. Results of EFAST first-order sensitivity analysis: (a) is fast first-order indexes; (b) is fast total order indexes.
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International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340
model response (Vohland and Jarmer, 2008). It was confirmed that Bt,
LAI, Psoil, Cab played an important role in the simulation of canopy
reflectance, during which parameters take measured values. Other less
sensitive parameters like N, Hspot, Cw and Cm took on fixed values after
optimization (Table 2). Optimization of insensitive parameters was
based on linear fit of measured canopy and simulated reflectance
(Table 2).
As illustrated by Fig. 5 and Table 3, the correlation coefficient of
simulated and measured reflectance reached 0.95, while RMSE and SD
were 0.045 and 0.046 respectively. Simulation results of different
spectral subsets indicated that the highest correlation existed between
subset-1(400–1349 nm) and simulated reflectance, where R2 was 0.96
and gave the lowest RMSE of 0.003. In the comparison between subset-2
(1452–1795 nm) and subset-3(2012–2400 nm), subset-2 showed mod­
erate correlation with measured reflectance, where R2 and bias were
0.91 and − 0.018, respectively. High correlation also existed between
subset-3(2012–2400 nm) and simulated reflectance, with R2 being 0.95.
In summary, the optimized parameters can simulate canopy reflec­
tance with a high degree of correlation. Moreover, the sensitive spectral
subset (530–550 nm) of Bt content showed a high degree (R2 = 0.96) of
match with measured reflectance, the vegetations has red pigment are
more sensitive to the 400 nm-560 nm spectral range(Prasad et al., 2012),
indicating that the optimization results are reliable.
3.2. Correlation between spectral indices and betalain contents
The sensitive spectral subset from the PROSAIL model was selected
for calculating of NDSI, NDPI, and RSI spectral indices on the basis of SA
analysis. Fig. 6 is the correlation map of the indices and Bt content ,
illustrating a significant correlation with the combined blue bands
(470–475 nm) with the correlation coefficient being 0.80.
As shown in Table 4 and Fig. 6, NDSI, NDPI, and RSI calculated by
the combination of simulated reflectance (R) 471 nm, 472 nm, 473 nm,
474 nm, and 475 nm indicated strong correlation with Bt content.
NDSI471nm,475nm, NDSI472nm,475nm, NDSI473nm,474nm, NDSI473nm,475nm;
NDPI471nm,475nm, NDPI472nm,475nm, NDPI473nm,474nm, NDPI473nm,475nm;
RSI471nm,475nm, RSI472nm,475nm, RSI473nm,474nm and RSI473nm,475nm
revealed a significant correlation with Bt content at 0.01p-value with the
average correlation being − 0.78,- 0.79, 0.80 (Table 4); and among these
indices, NDSI473nm,475nm, NDPI473nm,475nm, and RSI473nm,475nm showed
the highest correlation with Bt content among these indices with its
correlation coefficient reaching ± 0.80 with p < 0.001. These indices
indicated low correlation with other parameters, especially RSI. Thus,
these indices were selected for establishing an estimation model for Bt
content.
R. Sawut et al. International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340

Fig. 5. Simulation results (a) and RMSE, BIAS (b) of the canopy reflectance.

sensitive simulated spectral subsets (460–592 nm) illustrated superior

Table 3
performance to other estimation models built by spectral indices with
BIAS and RMSE of the simulated canopy reflectance by PROSAIL model.
highest validation coefficients R2 = 0.82, RMSE = 0.38 μg⋅cm− 2 and
Spectral subset R2 RMSE BIAS SD RPD = 2.12.
Subset-1 0.96 0.0026 0.0026 0.05 As for the model PROSAIL-SVM built by spectral indices, the
Subset-2 0.91 0.0184 − 0.0184 0.01 PROSAIL-NDSI-SVM model showed reliable performance albeit with
Subset-3 0.95 0.0017 − 0.0017 0.01
higher RMSE (0.58 μg⋅cm− 2) and lower R2 (0.52) and RPD value (1.54),
Total 0.95 0.0451 0.0451 0.46
while for the PROSAIL-RSI-SVM model promising prediction capability
was achieved with high R2 (0.71) and low RMSE (0.42 μg⋅cm− 2) and
3.3. Estimation accuracy of betalain contents RPD of 1.89 (Fig. 7). The model constructed using NDPI indices achieved
moderate prediction quality with R2 (0.65) and higher RMSE (0.49
The SVM estimation model was constructed on the basis of the μg⋅cm− 2). The best performing model used indices (NDPI473, 475,
simulated canopy reflectance. Estimation results indicated that cali­ NDSI473, 475 and RSI473, 475) with Bt content resulting in the highest R2
bration of five models obtained R2 values from 0.52 to 0.82, with RMSE (0.78) and lowest RMSE (0.39 μg⋅cm− 2).
values ranging from 0.38 μg⋅cm− 2 to 0.58 μg⋅cm− 2 and RPD values from
1.54 to 2.12 (Fig. 7). The PROSAIL + SVM model constructed by

Fig. 6. Three-dimensional maps demonstrating the correlation (r) between Bt content and the spectral indexes calculated from simulated reflectance.

7
R. Sawut et al. International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340

3.4. Spectral scale conversion and inversion model

Table 4
Correlation analysis between hyperspectral indices and PROSAIL parameters Simulated hyperspectral reflectance derived from the PROSAIL
(mean correlation values). model was converted into the multispectral Sentinel-2A reflectance
Index Bt Cab LAI Psoil (Fig. 8) on the basis of spectral responses of Sentinel-2A and formula
NDSIs − 0.78 − 0.33 − 0.29 − 0.17 (12). The figure given indicates the correlation between observed and
NDPIs − 0.79 − 0.27 − 0.23 − 0.20 simulated reflectance of the Sentinel-2A with an average correlation
RSIs 0.80 0.21 − 0.14 − 0.11 coefficient reaching 0.88, p < 0.001. Correlation of simulated bands
Not: NDSIs, NDPIs, and RSIs were calculated by high correlated spectral bands with Blue, Green, Red, vegetation red and NIR bands reached 0.92.
with Bt contents 471 nm,457 nm; 472 nm,474 nm; 472 nm,475 nm; 473 nm,474; Other bands (B1, B9, B10, B11, and B12) showed moderate correlation
473 nm,475 nm; 474 nm,475 nm, respectively. with coefficients being around 0.86.
For the selection of the sensitive Sentinel-2A bands of Bt content, the
global SA was applied. Results indicated that Bt exerts significant in­
fluence on Blue (B2) and Green (B3) whose contribution rate reached

Fig. 7. Scatterplots of measured Betalain content versus estimated Betalain content by SVM-PROSAIL.

Fig. 8. Simulated sentinel-2A reflectance. ((a) Represents – simulated Sentinel − 2A bands reflectance; (b) Represents –fitness level of observed and simulated
Sentinel bands).

8
R. Sawut et al.
66% and 68% respectively (Fig. 9). Furthermore, LAI is more sensitive to
Red (B4), vegetation red edge (B5, B6, B7), NIR (B8) and short-wave
infrared SWIR (B11) with contribution rates being about 30%～42%.
Psoil significantly affects B1, B5, B8, B9 and B10 with contribution
ranging from 65% to 80%. A low contribution of 2.4% to all of Sentinel-
2A bands was shown among other parameters such as Cw and Cm, while
Cab and N are sensitive to the Red band (24%, 20%). The sum of the
EFAST first order sensitivity coefficients (Cab, Bt, Cw, LAI, N, Psoil, and
Cm) was around 103%, with the exception of B1, B2, B6, B11 (100%).
This indicated that interactions of the parameters show correlation with
most of the Sentinel-2A bands to some extent.
Therefore, the bands B2 and B3 were selected as explanatory vari­
ables for the establishment of SVM inversion models. Python 3.7 was
used to run the SVM prediction model, with the test size being 0.2,
random state 100, and the number of predicted samples 51.
Two different models were constructed for inversion. Model-a built
using the most sensitive bands (B2, B3) while Model-b was built by
spectral indices (NDSI, NDPI, RSI) derived from Sentinel-2A sensitive
bands. These spectral indices were significantly correlated with Bt
content, particularly with RSIb2,b3 where the correlation reached 0.69
(Table 5). Inversion results of Bt contents were shown in the Fig. 10.
As shown, Model-a demonstrated good performance with high vali­
dation coefficients R2 = 0.64, RMSE = 0.47 μg⋅cm− 2 and RPD = 1.70,
while Model-b displayed robust estimation abilities with the highest R2
= 0.68, lowest RMSE = 0.44 μg⋅cm− 2 and highest RPD (1.75). From the
inversion map (Fig. 10), it can be concluded that the spatial distribution
of Bt content derived from Model-b was closer to that of the sampling
site.
It is possible to invert Bt content through multispectral remote
sensing, and spectral indices NDSIb3, b4, NDPIb3,b4, RSIb3,b4 (Fig. 10).
Compared to the hyperspectral model accuracy, it is obvious that Bt has
very limited sensitive bands, so that when carrying out spectral con­
version, soil humidity and other vegetation parameters may have
increased interference (Prasad et al., 2012; Wang et al., 2015), making
the multispectral model accuracy lower than the hyperspectral model
(Fig. 7, Fig. 10).
Fig. 9. EFAST first order sensitivity analysis of Sentinel − 2A bands in the
PROSAIL model.
9
International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340
Table 5
Correlation between Sentinel-2A spectral indices and the model parameters.
NDSIb2,b3 NDPIb2,b3 RSIb2,b3
Bt − 0.66 − 0.64 0.69
Cab − 0.23 − 0.27 0.21
LAI − 0.31 − 0.29 − 0.16
Psoil − 0.18 − 0.11 − 0.14
N − 0.07 − 0.09 0.07
Cm 0.002 0.001 0.001
4. Discussion
4.1. Estimation accuracy
Estimation and inversion of Bt content were realized on the basis of
the PROSAIL model and the SVM model and the spectral indices
(NDPI473, 475, NDSI473, 475 and RSI473, 475 and NDSIb2, b3, NDSI b2, b3, and
RSI b2, b3) were proposed on different spectral resolution. It was found
that the model (PROSAIL + SVM model) based on the simulated
hyperspectral canopy reflectance displayed robust estimation ability
(R2 = 0.82). The model built by spectral indices(calculated by sensitive
simulated reflectance) showed promising performance (R2 = 0.78). As
far as is known, this provides a novel study in the investigation of esti­
mating Bt content at a good accuracy based on a combination of the SVM
model and PROSAIL model at the different spectral scales. Estimation of
different leaf pigments (chlorophyll-a and-b, anthocyanin and carotene)
and other biochemical content (protein, cellulose, and lignin) and uti­
lization of inversion of a radiative transfer model have been regarded as
possible (Wang et al., 2015; Wang et al., 2016; Yao, 2015; Feret et al.,
2011), since the various pigments in the leaves are present in the optical
spectra of the leaf tissue. Description of the effects of leaf pigments,
moisture, structural parameters and other factors on the leaf retrore­
flective spectrum by the PROSPECT model can be used to quantitatively
obtain content of various components inside the leaf (Baret et al., 1992).
Wang et al.(2015) estimated the leaf protein and cellulose content on the
basis of the PROSPECT model, the coefficient of determination, R2
reached 0.83, and leaf reflectance was accurately constructed by the
radiative transfer model with newly calibrated specific absorption co­
efficients. Wang et al.(2016) estimated the carotenoid content with high
R2 (0.83) based on the PROSPECT model, and found estimation of
RVIDNDVI to carotenoid content could be verified with validation using
both simulated and measured data. The radiative transfer model has
physical function compared to other methods, it is variable parameter­
isation is flexible and simulated data has become the main data source to
perform inversion of vegetation biochemical parameters (Wang et al.,
2016).
4.2. Calibration of the PROSAIL model
Sensitivity analysis indicated that Bt, LAI, Psoil, Cab had significant
correlation with canopy reflectance, while Cw, N, Cm, and Hspot have less
with their sensitivity indexes around 0–0.2. Sensitivity can be applied to
describe the degree of influence of a variable on the output of the model
in the process of changing in phase (Li and Zheng, 2014). Some less
sensitive parameters can be fixed during the simulation. Zhang et al.
(2017) fixed some insensitive parameters such as Psoil, N, Car, Hspot
during the simulation of typical subtropical forest canopy reflectance by
PROSAIL, by which the simulation accuracy reaching approached 0.99
(R2). It was based on the simulated hyperspectral reflectance which
further simulated MODIS reflectance and obtained reliable results (R2 =
0.93). Lei et al.(2019) simulated the reflectance of green cream vege­
table, roman lettuce, and guangfu vegetable leaves on the basis of Cab,
Car, N parameters which are sensitive to 400–780 nm. The correlation of
measured reflectance was about 0.97. Wang et al.(2015) only used the
Cw, protein, and cellulose + ligin for simulation of fresh and dry leaf
R. Sawut et al.
Fig. 10. Scatterplots of measured Betalain content versus estimated Betalain content by SVM-PROSAIL (Sentinel-2A).
reflectance, and simulation accuracy of spectral subset1 (1100–2500
nm), subset4 (1020 nm, 1510 nm, 1730 nm, 1980 nm, 2060 nm) and
subset5 (1120 nm,1200 nm,1420 nm,1450 nm,1490 nm, and so on)
reached 0.96. Jing et al. (2012) based on the PROSPECT-5B model,
simulated three different satellites (ZY-3 MUX, GF-1WFV) reflectance,
and N, Cm, Cw, Car, and Cbrown, were fixed during the simulation for
reduction of the complexness and improvement of the potency of the LAI
inversion. And high inversion results were achieved for the ZY-3 MUX
simulated reflectance. The simulation results of our research demon­
strated that the simulated and measured reflectance correlation reached
0.95. Moreover, the spectral subset-1 (400–1349 nm) had the highest
correlation with simulated reflectance (R2 = 0.96) with the lowest RMSE
(0.002). The spectral subset-2 (1452–1795 nm) and subset-3
(2012–2400 nm) showed moderate correlation with R2 being 0.91 and
0.95, respectively. The simulated Sentinel-2A reflectance provided
strong correlations (R2 = 0.88, p < 0.001, among them correlation of
Blue, Green, Red, and vegetation red and NIR bands with observed-
sentinel bands reached 0.91 (Fig. 8). The specific sensitive spectral
subsets (460–592 nm) and Sentinel-2A bands (B2, B3) of betalain were
successfully obtained (Fig. 9).
10
International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340
4.3. Inversion accuracy of PROSAIL + SVM model
Due to the complexity of the radiation transmission model, the
nonlinear relationship between plant spectrum and leaf pigment con­
tent, the presence of many uncertain factors in the surface environ­
mental system, and the ill-posed inversion process in nature, the
traditional radiation transmission model inversion technology has been
unable to meet requirements of accurate estimation of vegetation
pigment content (Lü, 2012). Thus, different methods are proposed to
solve the inversion problem of the radiative transfer model. Tang et al.
(2011) applied the PROSAIL model for simulation of the reflectance
spectrum of soybean canopy. Their use of the RBF neural network hel­
ped them obtain good estimation results with the correlation coefficient
being 0.87. Lü (2012) leveraged combinations of the PROSAIL model
and machine learning models for the estimation of chlorophyll content
and found the RF-PROSAIL model achieved the highest chlorophyll
estimation accuracy compared with the GBM-PROSAIL. The computa­
tion time of RF-PROSAIL was less than that of GBM-PROSAIL, and
therefore, the RF-PROSAIL model was more suitable to crop chlorophyll
content estimation at the canopy level. Darvishzadeh et al.(2012)
inverted the PROSAIL model with application of the lookup table
method to predict the chlorophyll content of rice from AVNIR-2 multi­
spectral data, it was shown that the model R2 reached 0.65 and RMSE
R. Sawut et al.
was 0.45. Durbha.(2007) combined SVM with the PROSAIL radiation
transmission model to obtain the LAI from MISR (multiangle imaging
spectroradiometer) images and reasonable results were achieved. The
root mean square error of red light and near-infrared was 0.64, and R2 of
red light was 0.50. The model constructed by simulated Sentinel-2A
bands (B2, B3) showed promising estimation abilities with R2 being
0.63. Many studies have illustrated the potential of satellite imagery for
the estimation of various biochemical content, such as chlorophyll, ni­
trogen, and protein by hyperspectral indices, in which high accuracy is
demonstrated (Wang et al., 2015; Zhao et al., 2018; Li et al., 2019). Thus
in this study, spectral indices were also considered. The calculation of
RSI, NDPI, and NDSI was based on the sensitive simulated reflectance,
and the results validated for the estimation of Bt content with NDPI473,
475, NDSI473, 475, and RSI473, 475 indices. Estimation results indicated
that NDPI473, 475, NDSI473, 475 and RSI473, 475 andNDSIb2, b3, NDSIb2, b3,
and RSI b2, b3 hold great potential for estimation of Bt content in
different spectral scales, with estimation accuracy(R2) reaching 0.78
(NDPI473, 475, NDSI473, 475 and RSI473, 475) at hyperspectral scale and
0.68 (NDSIb2, b3, NDSIb2, b3 and RSI b2, b3) at multispectral scale.
Inverting Bt content was carried out and the estimation map was ob­
tained. It is confirmed that coupling the radiative transfer model and the
SVM model can solve ill-posed problems to some extent, along with the
successful estimation of some non-photosynthesis pigments. In turn,
development and demonstration of essential biodiversity variables used
for assessment of biodiversity, can be supported by such monitoring
(Pereira et al., 2013; Wang et al., 2015; Lü, 2012; Casa et al., 2019).
5. Conclusion
This study demonstrates the potential of combining the PROSAIL
model and SVM model in the estimation and inversion of the betalain
natural pigment content at the canopy level. Among the PROSAIL model
parameters Bt, LAI, Psoil, Cab exhibit significant correlation with canopy
reflectance of wetland vegetable (Suaeda salsa), with the Bt content
more sensitive to the spectral range 460–592 nm, where the sensitivity
index value reached approximately 70%. Optimized spectral indices
calculated from sensitive spectral bands (NDSI473nm, 475nm, RSI473nm,
475nm, and NDPI473nm,475nm) indicated high correlation with Bt
(R=±0.80 with p < 0.001). The PROSAIL + SVM model built by simu­
lated hyperspectral reflectance estimated Bt content with high R2 (0.82),
and the model constructed from NDSI473nm,475nm, RSI473nm,475nm and
NDPI473nm,475nm displayed promising predictive ability with high R2
(0.78). After spectral conversion, Bt content showed high correlation
with Sentinel-2A Blue, Green, Red, and vegetation red and NIR bands (R
= 0.91). The extension of the PROSAIL + SVM model to the multi­
spectral image (Sentinel-2A) showed moderate to a good prediction. The
spatial distribution map of Bt content by NDPIb2, b3, NDSIb2, b3, RSIb2, b3
indices was similar to the actual distribution. While Bt alone would not
only yield valuable information about the plant growing status, it could
be used to indicate changes in its growth environment, thus the study
may has significance in monitoring the natural pigments changes for the
response of the environmental changes at region scale.
CRediT authorship contribution statement
Rukeya Sawut: Data curation, Writing - review & editing. Ying Li:
Supervision. Yu Liu: Supervision, Investigation. Nijat Kasim: Software,
Validation. Umut Hasan: Writing - review & editing. Wei Tao:
Investigation.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
11
International Journal of Applied Earth Observations and Geoinformation 100 (2021) 102340
Acknowledgements
The authors are very grateful for the financial support provided by
National key R & D program of China (Grant No. 2017YFC0211904 and
2020YFE0201500). We also thank the Navigation College and Envi­
ronmental Information Institute of Dalian maritime university for their
support in providing data and discussion during the research. We are
extremely thankful to an anonymous reviewer and editor for valuable
comments that have greatly improved the clarity of this article
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