ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122

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ISPRS Journal of Photogrammetry and Remote Sensing

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Spectroscopic remote sensing of plant stress at leaf and canopy levels

using the chlorophyll 680 nm absorption feature with continuum
removal
Ieda Del’Arco Sanches a,b,⇑, Carlos Roberto Souza Filho b, Raymond Floyd Kokaly c
a
Remote Sensing Division (DSR), Brazilian National Institute for Space Research (INPE), Av dos Astronautas, 1758, Jd da Granja, CEP 12227-010 São José dos Campos, SP, Brazil
b
Institute of Geosciences, University of Campinas (UNICAMP), P.O. Box 6152, 13083-970 Campinas, SP, Brazil
c
U.S. Geological Survey, MS 973 Box 25046, Denver Federal Center, Denver, CO 80225, USA

a r t i c l e i n f o a b s t r a c t

Article history: This paper explores the use of spectral feature analysis to detect plant stress in visible/near infrared
Received 12 June 2014 wavelengths. A time series of close range leaf and canopy reflectance data of two plant species grown
Received in revised form 19 August 2014 in hydrocarbon-contaminated soil was acquired with a portable spectrometer. The ProSpecTIR-VS air-
Accepted 26 August 2014
borne imaging spectrometer was used to obtain far range hyperspectral remote sensing data over the
field experiment. Parameters describing the chlorophyll 680 nm absorption feature (depth, width, and
area) were derived using continuum removal applied to the spectra. A new index, the Plant Stress Detec-
Keywords:
tion Index (PSDI), was calculated using continuum-removed values near the chlorophyll feature centre
Hyperspectral
Airborne sensor
(680 nm) and on the green-edge (560 and 575 nm). Chlorophyll feature’s depth, width and area, the PSDI
Chlorophyll absorption feature and a narrow-band normalised difference vegetation index were evaluated for their ability to detect
Continuum removal stressed plants. The objective was to analyse how the parameters/indices were affected by increasing
Spectral feature analysis degrees of plant stress and to examine their utility as plant stress indicators at the remote sensing level
Vegetation index (e.g. airborne sensor). For leaf data, PSDI and the chlorophyll feature area revealed the highest percentage
(67–70%) of stressed plants. The PSDI also proved to be the best constraint for detecting the stress in
hydrocarbon-impacted plants with field canopy spectra and airborne imaging spectroscopy data. This
was particularly true using thresholds based on the ASD canopy data and considering the combination
of higher percentage of stressed plants detected (across the thresholds) and fewer false-positives.
Ó 2014 International Society for Photogrammetry and Remote Sensing, Inc. (ISPRS). Published by Elsevier
B.V. All rights reserved.

1. Introduction stress condition, should improve significantly (Carter, 1994;

Plant stress can be defined as any disturbance that adversely
influences plant growth (Jackson, 1986). It is caused by unfavour-
able environmental conditions such as lack of nutrients, water
deficiency, diseases, insect damage, and pollution. It would be
extremely helpful for farmers, foresters and ecologists worldwide
to be able to detect unhealthy plants as early as possible. In the
past decades, remote sensing has proved its utility for monitoring
vegetation, and with the recent advances in airborne imaging spec-
trometers, the capability to characterise plant canopies, including
⇑ Corresponding author at: Remote Sensing Division (DSR), Brazilian National
Institute for Space Research (INPE), Av dos Astronautas, 1758, Jd da Granja, CEP
12227-010, São José dos Campos, SP, Brazil.
E-mail addresses: ieda@dsr.inpe.br (I.Del’Arco Sanches), beto@ige.unicamp.br (C.
R. Souza Filho), raymond@usgs.gov (R.F. Kokaly).
Thenkabail et al., 2011).
Mapping and monitoring vegetation stress is useful for several
applications. The early detection of plant stress is critical to avoid
yield losses in crops (e.g. Zarco-Tejada et al., 2009) and in forests
(e.g. Eitel et al., 2011). Vegetation stress along with other factors
such as species composition and the spatial distribution of carbon
stocks can improve the understanding of ecosystem processes
(Swatantran et al., 2011). Metal induced vegetation stress can be
used to monitor phytoremediation of contaminated soils (e.g.
Rathod et al., 2013). Plant stress can be applied as an exploration
method for gas and oil hydrocarbon seepage (Noomen et al.,
2012; Lammoglia and Souza Filho, 2013). Detection of oil-induced
vegetation stress can be used to localize the space distribution of
oil spills on land (e.g. Li et al., 2005 and Khanna et al., 2013). Veg-
etation status can be used as an indirect indicator of underground
pipeline leakages (e.g. Sanches et al., 2013a,b).

http://dx.doi.org/10.1016/j.isprsjprs.2014.08.015
0924-2716/Ó 2014 International Society for Photogrammetry and Remote Sensing, Inc. (ISPRS). Published by Elsevier B.V. All rights reserved.
112 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122

In general, all plants seem to respond to stress in a similar way pasture nutrients (e.g. Mutanga et al., 2004; Sanches et al.,
(e.g. decline in growth rate and in the rate of acquisition of all 2013c) and to estimate pasture biomass (e.g. Mutanga and
resources) regardless of the source of the stress (Chapin, 1991). Skidmore, 2004). Noomen et al. (2008) have tested 51 hyperspec-
Carter (1993) examined eight stress agents among six plant species tral indices for detecting changes in maize and wheat canopy
and the results indicated that physiological responses to stress do reflectance as a result of underground natural gas leakage. Most
not vary much for different stressors. De Jong et al. (2012) analysed indices approached were ratios using visible and near-infrared
the spectral response of Mediterranean species submitted to five bands. Only a few indices were based on shortwave infrared bands.
different types of stress, and the spectral signs observed were the The continuum removal technique was not explored in their work.
same independently of the stressor. Sanches et al. (2013b) found Following the same reasoning, but with the purpose to detect
that three different plant species grown over contaminated soils plant stress, a new index, the Plant Stress Detection Index (PSDI),
had similar spectral behavior. They found that the red edge (spec- is introduced here. The PSDI is calculated based on a ratio of values
tral region of rapid change in reflectance of vegetation between the on the green edge of the chlorophyll 680 nm feature relative to the
visible red and the near infrared range – 680–740 nm) showed a centre of the feature. The objective of this work is to assess the
shift of its highest peak towards shorter wavelengths, followed capability of spectral feature analysis of the chlorophyll absorption
by a decrease in its gradient. Although similar physiological and feature, in general, and the PSDI, specifically, to detect plant stress.
spectral trends are in general observed for vegetation under stress, Absorption feature parameters (depth, width, and area) and PSDI
recent study found different physiological responses in plants values of healthy and stressed plants are calculated and compared
exposed to explosives (grown over soil contaminated with TNT for leaf and canopy spectra measured in areas of vegetation
or RDX) compared to those experiencing natural stress (i.e. drought affected by increasing amounts of hydrocarbon contamination.
and salinity) (Zinnert et al., 2013). Comparisons with a hyperspectral vegetation index (HVI) (i.e. nar-
The increase of reflectance in visible wavelengths is the most row band NDVI) are also presented. For that purpose, leaf and can-
consistent expression in leaf reflectance to plant stress (Carter, opy field data and ProSpecTIR-VS imaging spectroscopy data
1993, 1994; Carter and Knapp, 2001), being commonly a conse- acquired from a field trial are used here to analyse the spectra of
quence of the reduction of leaf chlorophyll concentration triggered a grass species and a leguminous species.
by the stress (Knipling, 1970). In plant stress studies, the red edge
is a common focus (e.g., Carter and Miller, 1994; Lamb et al., 2002;
Zarco-Tejada et al., 2003). Plants under stress normally present a 2. Materials and methods
blue shift of the red edge position (e.g. Filella and Penuelas,
1994; Jago et al., 1999; Smith et al., 2004; Sanches et al., 2013b). The spectral data analysed in this study were acquired from a
The 680 nm corresponds to the photosystem II light reaction cen- field trial conducted in an experimental area of the University of
tre, known as P680. Several vegetation indices explore the Campinas (CPQBA-UNICAMP), in the locality of Paulinia, Sao Paulo
680 nm feature, such as the Normalized Pigment Chlorophyll Index State, Brazil, in 2010. The experiment consisted of three planting
(NPCI) (Penuelas et al., 1994), the Plant Senescence Reflectance slots (Fig. 1) with dimensions of 60 m (length)  5 m (width), in
Index (PSRI) (Merzlyak et al., 1999) and the Simple Ratio Pigment which five vegetal species were grown, including the forages
Index (SRPI) (Penuelas et al., 1995). P680, along with the photosys-
tem I light reaction centre (known as P700; also named for its
absorption peak), are key pigments in the photochemical reactions
of plant photosynthesis (Hoefnagels, 2011). For remote sensing
applications (i.e. airborne or spaceborne) the advantages to explore
the visible/near infrared part of the electromagnetic spectrum are
that this region is less affected by atmospheric absorption and
measurements, typically, have greater signal-to-noise ratio than
other parts of the reflected solar wavelength region.
Spectral transformations and vegetation indices have been used
intensively in an effort to eliminate or reduce effects not related to
the target’s properties of interest and to enhance spectral features.
The continuum removal transformation consists of estimating the
absorptions not due to the chemical bond of interest and removing
their effects (Clark and Roush, 1984). The continuum removal
method was initially used in geological remote sensing and was
first applied to studies of leaf biochemistry by Kokaly and Clark
(1999). Continuum-removed spectra of plants have been further
normalised to relate changes in shapes of absorption features to
the abundance of a specific biochemical, for example, nitrogen
(Kokaly, 2001), by ratioing of the depths within absorption features
to the depth at the centre of the feature. This procedure minimises
the influence of factors such as atmosphere absorptions, soil back-
ground and leaf water, improving spectral feature analysis of veg-
etation canopies. Later, Mutanga et al. (2004) develop other two
indices based on feature depths, which were denominated the Nor- Fig. 1. True colour composition image produced from ProSpecTIR-VS data acquired
malised Band Depth Index (NBDI) and the Continuum-Removed over the area used in the experiment (Paulinia, Brazil). The three planting slots
Derivative Reflectance (CRDR). Parameters derived from contin- (60 m  5 m), corresponding to the control (CTR) and plants stressed by the
application of diesel (DSL) and gasoline (GSL) into the soil, are outlined on the
uum removal of plant absorption feature have been used to esti-
image in blue rectangles. The gray lines represent the thresholds between four
mate biochemicals of dry leaves (e.g. Kokaly and Clark, 1999; repetitions/parcels of the trial (P1–P4). In each parcel, the plots (3 m  5 m)
Curran et al., 2001), to discriminate vegetation types (e.g. Kokaly corresponding to the brachiaria (BR) and perennial soybean (PS) plants are
et al., 2003; Schmidt and Skidmore, 2003), to predict canopy highlighted in red and yellow dashed rectangles, correspondingly.
 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122
brachiaria grass (Brachiaria brizantha H.S.), hereafter referred to as
BR, and perennial soybean (Neonotonia wightii Am.), from now
referred to as PS. The soil used in the experiment is a eutroferic
red latosol with 65% of clay. During the test, forced flows of diesel
(DSL) and gasoline (GSL) were applied to the soil of two of the slots,
triggering plant stress. The plants in the third slot were not submit-
ted to any type of stress, and they were used as the control (CTR)
treatment. All plots were watered equally throughout the trial.
The experiment was conducted over a period of 6 weeks, from
19th April to 29th May 2010 (refer to Sanches et al. (2013b) for
more details about the experiment). In each slot, four plots
(parcels) of the abovementioned species were planted (P1–P4)
(Fig. 1). The first contamination was produced when all plant spe-
cies were well developed (i.e., the canopy was fully developed). The
experiment was ceased when the majority of the plants in the DSL
and GSL plots were visually highly stressed.
Leaf and canopy spectra of healthy and stressed brachiaria
and perennial soybean plants were obtained from field and air-
borne platforms. Three other cultures were planted during the
experiment but were not analysed in this study for divergent
reasons. The sugarcane plants grew taller than the height of
the mobile platform used to acquire the canopy data, compro-
mising the spectral measurements of this specie. The beans were
highly affected by the contaminations and almost no plant
survived to be measured simultaneously to the others. Maize
was also discarded based on previous analysis (Sanches et
al., 2013b); this issue is further mentioned in the manuscript
(see Section 4).
2.1. Acquisition of in situ vegetation spectra
Field (leaf and canopy) spectral measurements were obtained
with a portable FieldSpecÒ 3 High-Resolution spectrometer, which
detects electromagnetic radiation in the spectral range between
350 nm and 2500 nm (ASD, 2011a). In this study, the spectral anal-
ysis was focused on the chlorophyll absorption feature centered
near 680 nm. In this region, the FieldSpecÒ 3 Hi-Res has a spectral
resolution of 3 nm (@ 700 nm) and a sampling interval of 1.4 nm. A
SpectralonÒ panel (Labsphere Inc.) was used as the reflectance
standard. The spectrometer was configured to average 25 measure-
ments for each record. This study focus on the chlorophyll
absorption feature centered near 680 nm, because previous
analysis (Sanches et al., 2013a) of this dataset showed that plant
stress induced by hydrocarbon contamination was first detected
in this absorption feature compared to other vegetation spectral
features.
To acquire spectra of the vegetation canopy in situ, a mobile
platform was used. During measurements, the spectrometer was
positioned on the platform at a distance of 3.65 m from the soil,
and its optical fiber operated with a 5° foreoptics. With this
arrangement, each measurement comprised a ground sampling
area of 30 cm diameter. For each spectral measurement (desig-
nated M1 to M9), 10 spectra were acquired from contiguous and
non-overlapping areas in the central portion of each of the four
parcels (replicates), plant species and treatments (CTR, DSL and
GSL). To ensure that throughout the field campaign the exactly
same plot area would be measured, ten marks were painted in
the top of the mobile platform, marking the right spot where the
FieldSpec should be placed.
To measure plant leaves (adaxial surface) spectra, an ASD plant
probe (contact probe) and an ASD leaf clip accessory (ASD, 2011b)
were coupled to the spectrometer. The sampling area measured
with these accessories corresponded to 10 mm of diameter.
The nine spectral measurements (M1 to M9) were acquired
along a period time of 40 days. This protocol allowed the spectral
characterisation a, at leaf and canopy level, of healthy plants
113
(CTR) and plants grown under increasing volumes of stress factors
(DSL and GSL) (Fig. 2).
2.2. ProSpecTIR-VS airborne imaging spectrometer
An image of the experimental area (Fig. 1) was acquired using
the ProSpecTIR-VS imaging spectrometer (SPECTIR, 2012), which
operates with Specim’s AISA dual sensors covering visible/near
infrared (VNIR) (400–970 nm; AISA Eagle) and shortwave infrared
(SWIR) (970–2500 nm; AISA Hawk) wavelengths. The image was
acquired on 15th May 2010, which is the corresponding date to
the canopy spectral measurement M8. The FotoTerra/SpecTIR com-
panies operated the sensor in Brazil. The imaging data were pro-
vided with 357 channels distributed among the VNIR (122
channels) and the SWIR (235 channels) at a spatial resolution of
0.6 m. In this study, only data from the VNIR sensor were used.
The spectral resolution ranged from 5 to 6 nm across the wave-
length range of the VNIR sensor. The data was available both at
radiance and 1A processing level (i.e. reflectance). In order to con-
vert the calibrated radiance data to surface reflectance values, the
software package ATCOR4 was employed using MODTRAN4 atmo-
spheric lookup tables to correct for atmospheric absorption and
scattering components (Richter and Schlapfer, 2012). Polishing of
the reflectance was achieved using a SpecTIR proprietary program
based on a Savitsky–Golay algorithm.
2.3. Spectral data processing and data analysis
The leaf and canopy spectra collected with the ASD spectrome-
ter were processed using the USGS PRISM software (Kokaly, 2011).
The data for each treatment (CTR, DSL, and GSL), species (BR and
PS), and measurement date (M1 to M9) were averaged. Each aver-
age spectrum was converted to absolute reflectance by removing
the absorption features of the Spectralon reference panel (Kokaly,
2011). Continuum removal (Clark and Roush, 1984) of the chloro-
phyll absorption feature centered near 680 nm was calculated
using adjusted continuum end points. In contrast, Kokaly et al.
(2003) used fixed continuum endpoints when analyzing the chlo-
rophyll feature for species discrimination. In the latest version of
the USGS PRISM software (available at ftp://ftpext.cr.usgs.gov/cr/
co/denver/kokaly/usgsprism/), endpoints used in continuum
removal can be tailored for each spectrum analysed.
Once the plots were visually inspected on the ProSpecTIR-VS
reflectance data (Figs. 1 and 3a), ten pixels were selected from
the middle portion of each plot (Fig. 3b) and reflectance spectra
extracted from them (Fig. 3c) and averaged. Twenty-four averaged
spectra were analysed, corresponding to three spectra per treat-
ment (CTR, DSL and GSL) in four repetitions (P1 to P4) for each
plant species (BR and PS). Then, the continuum-removed reflec-
tance spectra for the chlorophyll absorption feature were obtained.
2.3.1. Absorption feature parameters
The continuum-removed spectrum (R0 ) is calculated by dividing
the original reflectance values within the spectral feature by the
corresponding values of a continuum line (Fig. 4a) established
between the two endpoints (left and right) of the feature. The
resultant absorption feature is characterised by the depth at the
feature centre (Dc) (i.e., the maximum feature depth), the feature
width (the full width at half maximum – FWHM) and the feature
area (Fig. 4b; see also Kokaly, 2011). Variations of these parameters
describe, in simple terms, the variation in the shape of an absorp-
tion feature. Here, the Dc, FWHM and area of the 680 nm chloro-
phyll absorption feature of healthy and stressed plants are
examined.
114 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122

Fig. 2. Spectra were obtained on nine dates of the field experiment. Measurements were accomplished for each plant group under investigation; i.e., plants not submitted to a
stress factor (CTR) and plants stressed by the application of increasing amounts of diesel (DSL) and gasoline (GSL) into the soil where they were grown.

Fig. 3. (a) Subset of the ProSpecTIR-VS true colour image shown in Fig. 1; (b) zoom
in a perennial soybean plot screening the location of the selected 10 pixels; (c)
example of perennial soybean spectra (n = 10) extracted from the imagery.

2.3.2. Plant Stress Detection Index (PSDI)
A new index based on the continuum-removed 680 nm
chlorophyll absorption feature is presented in this study. In the
continuum-removed reflectance spectra (Fig. 4b), the continuum-
removed reflectance at the feature centre (R0 c) is the minimum R0
value in the continuum-removed absorption feature (Fig. 4b). This
parameter is used in the PSDI formula (Eq. (1)), as follows:
PSDIðiÞ ¼ ðDðiÞ  R0c Þ=ðDðiÞ þ R0c Þ
where the feature depth (D) (Fig. 5a–c) of each channel i in the
absorption feature is computed by (Eq. (2)):
DðiÞ ¼ 1  R0ðiÞ
PSDIs calculated for the chlorophyll 680 nm absorption features
of brachiaria leaf and canopy spectra are illustrated in Fig. 5b and d,
respectively. In Fig. 5, the arrows in the plots (arrows of the same
colour have the same length) show how the PSDI enhances the dif-
ferences between healthy and unhealthy plants. In PDSI produced
from leaf spectra this difference is doubled in the wavelengths
around 575 nm and in PSDI derived from canopy spectra the differ-
ence is even more substantial around 560 nm. Accordingly, for
plant stress detection it is necessary to calculate the PSDI for only
one wavelength, depending if a leaf (Eq. (3)) or canopy spectrum is
used (Eq. (4)):
Fig. 4. (a) Example of a brachiaria spectrum extracted from the ProSpecTIR-VS
image showing the continuum line over the chlorophyll absorption feature centred
near 680 nm and (b) the continuum-removed 680 nm feature.
Leaf PSDI575 ¼ ðDð575nmÞ  R0c Þ=ðDð575nmÞ þ R0c Þ ð3Þ
Canopy PSDI560 ¼ ðDð560nmÞ  R0c Þ=ðDð560nmÞ þ R0c Þ ð4Þ
These wavelengths (575 nm, 560 nm) were specified based on
ð1Þ the PSDI data of healthy plants (control) analysed.
The performance of the proposed index was assessed by com-
paring the results of plant stress detection based on the parameters
of the 680 nm chlorophyll absorption feature (Dc, FWHM and Area)
ð2Þ with the PSDI results. In addition, a comparison was also made
with the most commonly used vegetation index, the Normalized
Difference Vegetation Index (NDVI) (Rouse et al., 1973) using nar-
row bands, which will be referred as HVI800–670 (Eq. (5)):
HVI800—670 ¼ ðRð800nmÞ  Rð670nmÞ Þ=ðRð800nmÞ þ Rð670nmÞ Þ ð5Þ
3. Results
3.1. Plant stress symptoms observed
Physiological (e.g. leaf colour) and morphological (e.g. leaf
droop) changes in plant can occur because of stress (Jackson,
 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122
Fig. 5. Examples of spectra extracted from healthy and stressed brachiaria. (a) Depth of the 680 nm chlorophyll absorption feature of an ASD leaf spectra and (b) the
corresponding PSDI. (c) Depth of the 680 nm chlorophyll absorption feature extracted from a ProSpecTIR-VS pixel and (d) the corresponding PSDI. Arrows of the same colour
have the same length.
1986). The stress caused to the brachiaria and the perennial soy-
bean plants, which were grown over soils contaminated with die-
sel or gasoline in this study, were leaf-yellowing, decrease of green
biomass, increase of dry matter and sparsening of the canopy cover
(Fig. 6). Weak growth, changes in leaveś structure accompanied by
chlorophyll degradation and consequently colour variation, falling
of leaves, lower density of plants and in extreme cases vegetation
death are effects previously observed on plants grown in soils con-
taminated by hydrocarbons (Smith et al., 2004; Souza Filho et al.
(2008); Lammoglia and Souza Filho, 2013).
3.2. Results for ASD leaf and canopy data analysis
The PSDI, HVI800–670, Dc, FWHM and area values per leaf and
canopy measurements (Fig. 2) are plotted in Figs. 7 and 8, respec-
tively. It is observed that for healthy plants (CTR) the indices/
parameters values do not present much variation, whereas for
stressed plants (DSL and GSL) there is a decrease in these values
as the duration and volume of the stress factor increases. As
expected, the trend observed for all indices and feature parameters
is overall very similar.
There is a high positive correlation among all the parameters/
indices analysed (Table 1). The highest correlation (1.00) was
observed between the PSDI and feature area and between
HVI800–670 and Dc. The feature area is also correlated to the feature
width (FWHM) and depth (Dc), whereas the FWHM and the Dc are
less inter-correlated.
The descriptive statistics of the parameters/indices are pre-
sented in Table 2. The canopy means were higher than the leaf
means, whereas the data variation (CV) was higher in leaf spectra
compared to canopy spectra.
Based on the variation observed in the brachiaria and perennial
soybean healthy plants, thresholds were set for each index/param-
eter to assess their capability to detect plant stress based on leaf
and canopy data, separately (Table 2). The most liberal threshold
115
tested was based on the minimum value. If the index/parameter
for a sample is less than the minimum (Min) index/parameter
value of the control group (CTR), then the sample refers to a
stressed plant. The other thresholds evaluated were the mean
value minus twice the standard deviation (Mean  (2 * SD)), the
mean value minus three times the SD (Mean  (3 * SD)) and the
minimum value minus the SD (Min  SD).
The percentages of stressed plants (i.e. number of samples in
the entire dataset identified as stressed plant), for time periods
M2–M9, detected by each index/parameter using the four thresh-
olds (Table 2) are presented in Table 3. For the ASD leaf data, con-
sidering the performance along all thresholds, the best results were
obtained with the PSDI575 and feature area (detection of 67–70% of
stressed plants). For the canopy data, the highest percentage of
stressed plants were detected with the FWHM (52%) when using
the most liberals thresholds (Min and Mean  (2 * SD)) and with
the PSDI560, HVI800–670 and Dc (35%) for the most conservatives
thresholds (Mean  (3 * SD) and Min-SD). Considering leaf and
canopy data results combined, the PSDI, followed by the FWHM,
had the best performance in detecting plant stress along the
thresholds.
The similar results obtained with the HVI800–670 and the Dc is in
accordance with the high inter-correlation of these two variables
(Table 1). The same was observed for PSDI and feature Area. How-
ever, the performance of the PSDI in detecting plant stress in can-
opy data was better than the area (Table 3). This is an indication
that with the PSDI the detection of the changes caused by the
stress in the chlorophyll absorption feature is more efficient.
The results for plant stress detection using the PSDI and the
Min-SD threshold are presented in Fig. 9. Brachiaria plant stress
was detected at leaf and canopy scales independent of the stress
factor type (diesel or gasoline). The same was noticed for leaf
perennial soybean. However only the plant stress caused by soil
contaminated with gasoline (GSL) was detected using perennial
soybean canopy data.
116 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122

Fig. 6. Examples of brachiaria and perennial soybean plots showing healthy and stressed plants.

Fig. 7. Leaf level PSDI, HVI800–670, Dc, FWHM and area trends for brachiaria and perennial soybean spectral measurements of healthy (CTR) and stressed plants (DSL and GSL)
using the ASD spectrometer.
 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122
Fig. 8. Canopy level PSDI, HVI800–670, Dc, FWHM and area trends for brachiaria and perennial soybean spectral measurements of healthy (CTR) and stressed plants (DSL and
GSL) using the ASD spectrometer.
Table 1
R-squares between absorption features parameters and indices for brachiaria and
perennial soybean leaf and canopy data. The highest and lowest correlations are
highlighted in light and dark gray, respectively.
3.3. ProSpecTIR-VS image
The PSDI, HVI800–670, Dc, FWHM and area calculated based on
the imaging spectrometer data are plotted in Fig. 10 along with
the M8 ASD canopy data (previously shown in Fig. 8). The M8
ASD spectral measurements were acquired in a date close to the
ProSpecTIR image acquisition. There is a good compatibility
between ASD and image canopy data. Again, the trend observed
117
for all indices and feature parameters is similar. Overall, the
healthy plants (CTR) indices/parameters values tend to be higher
than the stressed plants (DSL and GSL) values.
The thresholds specified based on the ASD canopy data (Table 2)
were applied to the ProSpecTIR-VS image data. The results are pre-
sented in Table 4. For the most liberal thresholds (Min and
Mean  (2 * SD)), false-positives (control plants classified as
stressed plants) were observed for all indices/parameters. For the
most conservative threshold (Min-SD), only the FWHM shows false
positives. Overall, the PSDI and Dc display the lowest number of
false-positives across thresholds. Between these two, the PSDI
yields the highest percentage of stressed plants detected.
The plots where plant stress was detected with the PSDI using
the most conservative threshold tested (Min-SD) are shown in
Fig. 11. The stress was detected in all GSL parcels independent of
plant species. For the DSL stress factor, the result was better for
brachiaria. Only one perennial soybean parcel was identified as
stressed. Field observations showed that plant stress caused by
the contamination of the soil with gasoline was more severe than
the stress caused by the contamination with diesel, mainly for the
perennial soybean canopy (Fig. 12).
4. Discussion
At first, observing the similar trends presented for all of the fea-
tures parameters and indices analysed (Figs. 7 and 8), it seemed
that the plant stress detection could be done with the same degree
of success independently of the parameter/index used. As men-
tioned earlier, this similarity results from the high correlation
among these parameters/indices (Table 1). It has been shown in
this work that the feature area, width and depth at feature centre
were reduced all together (proportionally), as the chlorophyll
absorption feature shrank by the decrease in light absorption
caused by the stress. Similarly, the PSDI and HVI800–670 values fol-
lowed this reduction, demonstrating their sensibility to these
parameters, in particularly to the feature area and maximum fea-
ture depth, respectively. However, when testing the parameters/
indices under different scenarios (i.e. thresholds and data type –
leaf or canopy, ASD or ProSpecTIR-VS), their efficiency as plant
118 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122

Table 2
Statistics for the ASD leaf and canopy control treatment (healthy brachiaria and perennial soybean plants) and thresholds
(highlighted in gray) for plant stress detection: minimum value (Min), mean value minus twice the standard deviation
(Mean  (2*SD)), mean value minus three times the SD (Mean  (3*SD)) and minimum value minus the SD (Min  SD) (leaf:
n = 46; canopy: n = 50).

LEAF
Min Max Range Mean SD CV Mean-(2*SD) Mean-(3*SD) Min-SD
PSDI575 0.06 0.50 0.44 0.26 0.17 0.66 -0.09 -0.26 -0.11
HVI800-670 0.65 0.80 0.16 0.72 0.06 0.08 0.60 0.55 0.59
Dc 0.72 0.85 0.13 0.79 0.05 0.06 0.69 0.65 0.67
FWHM 117 137 20 130 6 0.05 119 113 111
Area 83 109 26 96 10 0.10 77 67 74
CANOPY
Min Max Range Mean SD CV Mean-(2*SD) Mean-(3*SD) Min-SD
PSDI560 0.19 0.74 0.55 0.54 0.16 0.30 0.22 0.06 0.02
HVI800-670 0.79 0.92 0.13 0.87 0.04 0.04 0.80 0.76 0.75
Dc 0.82 0.94 0.11 0.90 0.03 0.04 0.83 0.80 0.79
FWHM 141 156 15 150 4 0.03 141 137 137
Area 108 140 32 127 9 0.07 109 99 98

Table 3 the VNIR range were used, such as AVIRIS-Classic (Green et al.,
ASD data. Percentage of stressed plants detected by each indices/parameters for the 1998) or HyMap (Cocks et al., 1998), thresholds would need to
thresholds tested: minimum value (Min), mean value minus twice the standard be established from the convolved spectra.
deviation (Mean  (2*SD)), mean value minus three times the SD (Mean  (3*SD)) The idea to develop the PSDI was to have an objective and sim-
and minimum value minus the SD (Min  SD). The best result for each threshold is
highlighted in gray (leaf: n = 46; canopy: n = 50).
ple methodology to detect plant stress. Both leaf and canopy spec-
tra were explored, but it was noticed that the usefulness of the
Min Mean-(2*SD) Mean-(3*SD) Min-SD PSDI was more relevant to canopy data analysis. For all thresholds
PSDI575 70% 67% 67% 67% evaluated, negative values of PSDI560 were related to plants under
HVI800-670 70% 67% 50% 67% stress. Thus, for this study, it can be stated that if a sample has a
LEAF

Dc 70% 67% 53% 67% canopy PSDI560 6 0, the sample refers to a stressed plant. In that
FWHM 67% 67% 67% 67% case there is no need to have control samples (healthy plants) to
Area 70% 67% 67% 67% compare to the unknown samples.
When spectral libraries are available, spectral feature analysis
PSDI560 48% 48% 35% 35%
can be applied using a fitting algorithm. Recently, Kokaly et al.
CANOPY

HVI800-670 45% 45% 35% 35%

(2013) have delineated oil contamination in marshes from the
Dc 42% 45% 35% 35%
Deepwater Horizon spill in the Barataria Bay by comparing AVIRIS
FWHM 52% 52% 32% 32%
data to reference spectra of oiled marsh. The two hydrocarbon
Area 48% 48% 32% 29%
absorption features centred near 1.7 lm and 2.3 lm were analysed
PSDI 59% 57% 51% 51%
LEAF +CAN.

using the Material Identification and Characterization Algorithm

HVI800-670 57% 56% 43%
Dc 56% 56% 44%
FWHM 59% 59% 49%
Area 59% 57% 48%
stress indicators varies, especially for canopy data. For the most
severe levels of plant stress, all indices/parameters performed
correspondingly (i.e. detected the stress), whereas for low and
intermediate levels of stress the performance can be diverse,
depending on data type (leaf or canopy), plant species and thresh-
old adopted. Overall, the performance of the PSDI was more robust
across the different situations and thresholds evaluated.
In this study, thresholds developed from the canopy reflectance
spectra measured with the ASD spectrometer were directly applied
to the ProSpecTIR-VS data. These spectrometers have similar char-
acteristics (sampling interval and bandpass) in the VNIR range,
allowing this direct application. To test this, the ASD measure-
ments were convolved to the sampling and bandpass characteris-
tics of the imaging spectrometer. The absorption feature
parameters and PSDI values computed from the convolved data
were within 1% of the values computed from original ASD spectra.
If imaging spectrometers with coarser sampling and resolution in
51% (MICA), a module of PRISM (Kokaly, 2011). To detect the post-
51% impact stress caused by such contamination, a simple approach,
49% such as the PSDI presented here, would seem to be a reasonable
49% way to examine ecosystem responses (similar to Khanna et al.,
2013).
Different wavelengths were specified for PSDI analysis of leaf
(575 nm) and canopy data (560 nm). Among the healthy plants
(CTR) considered here, none presented negative values of PSDI
from these bands until the feature centre at around 680 nm (exam-
ple in Fig. 5b and d). The 560 nm and 575 nm appeared among the
wavelengths ranges (535–640 nm 685–700 nm) most sensitive to
stress when analysing leaf spectra of plants submitted to different
types of stress (Carter, 1993). As presented in Table 2, the length
(FWHM) of the chlorophyll absorption feature is wider in canopy
spectra (141–156 nm) than in leaf spectra (117–137 nm). This is
the reason why the canopy PSDI uses a shorter wavelength as a
key. In fact, the PSDI575 could be used to detect stress at canopy
level as well, but the detection would not be as efficient as that
provided by the PSDI560.
The HVI800–670 was the only parameter/index analysed that was
not calculated based on the continuum-removed reflectance. Sim-
ilar results were yielded with the HVI800–670 and the chlorophyll
feature depth at the feature centre (Dc). For the most conservative
threshold when analysing leaf data (Mean  (3 * SD)), the worst
 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122 119

Fig. 9. Results for plant stress detection using the PSDI and the threshold Min-SD for leaf and canopy brachiaria and perennial soybean data. If the PSDI value for a sample is
less than the minimum index value of the control group (CTR), then the sample is stamped as a stressed plant. No stress – the plant is not stressed because it was not exposed
to any type of contaminant (including DSL M1 and GSL M1 which were measured before the first contamination was done). Stress not detected or not stressed yet – the plant
was exposed to the contaminant (diesel or gasoline) but it does not show any sign of stress yet or the stress was not detected with the PSDI. Stress detected – the plant was
stressed because it was exposed to the contaminant and the stress was detected.

Fig. 10. ProSpecTIR-VS-based PSDI, HVI800–670, Dc, FWHM and area for brachiaria and perennial soybean canopies for each plot (P1 to P4) of healthy (CTR) and stressed plants
(DSL and GSL). Values plotted in red asterisks correspond to the ASD-based values for canopy data from M8, acquired on a date near the image acquisition.

Table 4
ProSpecTIR-VS data. Percentage of stressed plants (n = 24), including both BR and PS, It is relevant to mention that during the experiment only one
detected (overall accuracy) by each indices/parameters for the thresholds determined ProSpecTIR-VS image could be acquired. Ideally, the availability
based on ASD canopy data: minimum value (Min), mean value minus twice the of several images, from the beginning to the end of the experiment,
standard deviation (Mean  (2*SD)), mean value minus three times the SD would make it possible to effectively evaluate the PSDI to detect
(Mean  (3*SD)) and minimum value minus the SD (Min  SD). For each threshold,
the results with smaller percentage of false-positives (commission error) are
plant stress using temporal remote sensing imagery. But that
highlighted in gray. was not possible due to budget constraints. The airborne survey
took place near the end of the experiment, when some plants
already exhibited high degrees of stress. However, the fact that
Percentage of stressed plants detected (percentage of false-posives)
Min Mean-(2*SD) Mean-(3*SD) Min-SD the stress on crop plots was detect using the PSDI (e.g. DSL-BR
PSDI563 81% (13%) 81% (13%) 81% (0%) 75% (0%)
and GSL-BR in parcel 2 (P2) – Fig. 11), particularly where the stress
HVI800-670 81% (25%) 88% (25%) 81% (13%) 81% (0%) symptoms were not visually evident (e.g. DSL-BR and GSL-BR in
Dc 81% (13%) 81% (13%) 81% (0%) 69% (0%) parcel 2 (P2) – Fig. 11), demonstrates the efficacy of the proposed
FWHM 94% (25%) 100% (25%) 81% (13%) 81% (13%) index.
Area 81% (25%) 88% (25%) 81% (0%) 75% (0%) The findings of this work were obtained with the evaluation of
two perennial plant species, the brachiaria grass (monocotyledon)
and the perennial soybean leguminous (dicotyledon) (Figs. 6 and
12). Mono and dicotyledons have distinct leaf structure (narrow
result in detecting plant stress were obtained with the HVI800–670 versus broadleaves) and arrangement (vertical versus horizontal),
(Table 3). Although for the Min-SD threshold the lowest percentage which are very relevant under the remote sensing perspective.
of false-positive and highest percentage of stressed plants detected Despite their differences, the PSDI at 560 nm (563 nm in PRoSpec-
in the ProSpecTIR-VS image was obtained with the HVI800–670, it TIR-VS image) could be used to detect plant stress in both plants.
was also with this index that the highest percentages of false-pos- For annual plants (e.g. maize, beans), which goes through a
itives were reached for the other three thresholds tested. sequence of development phases in a rather short period (few
120 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122
Fig. 11. ProSpecTIR-VS image (channel 563 nm) in grey scale. The blue rectangles
delimit the planting slots (CTR healthy plants and DSL/GSL stressed plants). In each
parcel (separated by the gray lines), the plots corresponding to the brachiaria (BR)
and perennial soybean (PS) plants are highlighted in red and yellow dashed
rectangles, correspondingly. The ‘‘S’’ in red identifies the plots where plant stress
was detected with the PSDI using the most conservative threshold tested (Min-SD).
months), the detection of stress using the PSDI at 560 nm might be
appropriate only for the first phases. When these plants reach their
physiologic maturity they show symptoms of stressed plants. As a
result, the detection of stress caused by external agents can be
Fig. 12. Photos of perennial soybean and brachiaria plots taken on M8 – a date close to the acquisition of the ProSpecTIR-VS image. Differences among healthy plants (CTR),
and plants stressed by the application of diesel (DSL) and gasoline (GSL) into the soil are clearly portrayed in the pictures.
mistaken by natural plant development (Sanches et al., 2013b).
Noomen et al. (2008) evaluated the correlation of different vegeta-
tion index with oxygen concentration in maize and wheat. Is was
not possible to find one reflectance index that could be used an
any time during the growth cycle of the plants due to the constant
change of canopy characteristics. A more sophisticated approach,
in which the threshold adjusts as a function of time and local tem-
perature and precipitation patterns should be postulated.
Considering the PSDI, Dc and area parameters, two threshold
(the most conservatives) predetermined based on ASD canopy data
could be successfully applied (i.e. no false-positives) to the imaging
spectrometer data. Based on the results shown here, it is clear that
a conservative constraint, such as the Min-SD, is necessary to min-
imise the chances of false-positives when detecting plant stress in
image data. Comparable results are expected to be obtained for
other airborne imaging spectrometers with resolution similar to
the ProSpecTIR-VS sensor.
4.1. Relevance of PSDI for hydrocarbon contamination detection and
future application with upcoming orbital hyperspectral missions
The objective of this paper was to evaluate general plant stress
detection using spectroscopic remote sensing focused on the con-
tinuum removal of the chlorophyll absorption feature. For that
purpose, the data from a field experiment where plants were
grown over soil contaminated by liquid hydrocarbons (gasoline
and diesel) were used. It is not the intention of the present docu-
ment to discuss the results for hydrocarbon contamination
obtained with the mentioned trial. Those results were previously
presented in Sanches et al. (2013a,b). However, since a new
method is proposed in this study it is relevant to make a comment
about it. Considering the ASD data, with the PSDI it was possible to
detect the plant stress in brachiaria and perennial soybean more
precociously (i.e. when the plants were submitted to lower levels
of contaminants) compared to the red edge position (Sanches
 I.D. Sanches et al. / ISPRS Journal of Photogrammetry and Remote Sensing 97 (2014) 111–122
et al., 2013b). This improvement in plant stress detection using the
PSDI was more significant when analysing the canopy data. This
finding is particularly interesting considering that the ultimate
goal is to detect canopy plant stress over remote platforms (air-
borne or spaceborne).
Although there is no orbital hyperspectral sensor with global
data acquisition capacity currently in operation, different initia-
tives are in progress for the planning, construction and launch of
this type of sensors. The EnMAP sensor (Environmental Mapping
and Analysis Program), under development by the German Aero-
space Center (DLR) in partnership with the German Research Cen-
tre for Geosciences (GFZ) (Kaufmann et al., 2012), should be
launched in 2018. NASA plans to launch HyspIRI (Hyperspectral
Infra-Red Imager) (Green et al., 2012) by 2023. There are also the
HISUI from Japan (METI), the PRISMA from Italy (ASI), the MSMI
from South Africa (SunSpace), the HYPXIM from France (CNES)
and the SHALOM from Israel and Italy (ISA/ASI) (Staenz and Held,
2012; Staenz et al., 2013). This constellation of satellites with
hyperspectral sensors will provide enough spectral resolution for
the application of the PSDI at global level.
Overall, the use of hyperspectral technology offers great poten-
tial for increasing knowledge on natural resources. Despite the rel-
ative high cost for data acquisition, there is no doubt about the
advantages offered by this technology. The advances in this field
will be possible as long as more research is conducted by an
increasing number of scientists in different regions of the planet
and this work represents a contribution to towards it.
5. Conclusion
For the management of natural environments or agricultural
areas, the detection of plant stress as early as possible has a great
value. It can allow an intervention to be made in time to control the
stress factor and to restrain damages. In this context, the method-
ology of exploring the chlorophyll absorption feature centred at
approximately 680 nm with the continuum removal technique
presented in this work proved useful. It was observed a progressive
decrease in the chlorophyll absorption width, depth and area val-
ues as the plants (DSL and GSL) were exposed to increasing levels
of contaminants (liquid hydrocarbons). Consequently, these
parameters have a potential to be used as plant stress indicators,
as well as indices based on them.
Considering the two plant species analysed (brachiaria and
perennial soybean), and all the thresholds tested, overall, the best
results for detecting stress in this study were obtained with the
PSDI and the feature area when analysing leaf data (67–70% of
stressed plants detected), and with the PSDI when exploring can-
opy spectra extracted from field (35–48% of stressed plants
detected) and airborne platforms (75–81% of stressed plants
detected). The ProSpecTIR-VS image analysed in this study was
acquired in one single date (M8), whereas the ASD canopy data
correspond to several dates (M1 to M9). That explains the higher
percentage of stressed plants detected based on the image. Also,
the sample size of the imagery data analysed (n = 26 samples)
was smaller than the sample size of the data collected in the field.
It would be advisable to apply the PSDI to other plant stress sit-
uations, including different types of plants and stress factors in an
experimental setup with a larger sample size, to extend the index
performance assessment. It would be also convenient to test the
methodology for other hyperspectral images. Nevertheless, the
results presented in this study for two species of perennial forage
(mono and dicotyledons) are an indication of the potential of spec-
tral feature analysis of the chlorophyll absorption feature parame-
ters (width, area and depth) and the PSDI as a plant stress
indicator.
121
To be able not only to detect but also to identify the cause of the
stress would be even more valuable. However this is not a simple
task as stressed plants present in general a similar reaction inde-
pendently of the nature of the stress, as demonstrated by other
researchers. The answer might be in the synergy of chlorophyll-
based approaches with analysis of absorption features in the
shortwave infrared wavelengths. For the time being, the remote
identification of plant stress type remains a challenge and a
important field to be researched.
Acknowledgements
I.D. Sanches is grateful to FAPESP for her post-doctorate schol-
arship (Processo FAPESP n. 2011/03416-8). The authors are thank-
ful to Wilson Oliveira (Petrobras) and Marcos Nopper Alves
(CPQBA-UNICAMP) for their innovative ideas and contributions
during the field experiments. We are greatly indebted to Luciola
Magalhaes and Giuliana Quiterio for their involvement with all
phases and aspects of the spectral measurements in the field. We
also acknowledge the researchers of the Technology Program for
Transport (PROTRAN) of the Research Center of Petrobras (CEN-
PES), especially to Pedro Altoe Ferreira, Lis Maria Leoni Rabaco
and Renato Seixas da Rocha, for the financial and logistic support
dedicated to the Biomarkers Phase-1 Project developed in partner-
ship with UNICAMP. C.R. Souza Filho acknowledges CNPq for the
research grant.
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