remote sensing

Review
Thermal Imaging for Plant Stress Detection and Phenotyping †
Mónica Pineda , Matilde Barón and María-Luisa Pérez-Bueno *

Department of Biochemistry and Molecular and Cell Biology of Plants, Estación Experimental del Zaidín,
Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain; [email protected] (M.P.);
[email protected] (M.B.)
* Correspondence: [email protected]; Tel.: +34-958181600
† This paper is dedicated to Prof. Hartmut K. Lichtenthaler, a pioneer in imaging techniques applied to plant
stress research in Europe.

Abstract: In the last few years, large efforts have been made to develop new methods to optimize
stress detection in crop fields. Thus, plant phenotyping based on imaging techniques has become an
essential tool in agriculture. In particular, leaf temperature is a valuable indicator of the physiological
status of plants, responding to both biotic and abiotic stressors. Often combined with other imaging
sensors and data-mining techniques, thermography is crucial in the implementation of a more
automatized, precise and sustainable agriculture. However, thermal data need some corrections
related to the environmental and measuring conditions in order to achieve a correct interpretation of
the data. This review focuses on the state of the art of thermography applied to the detection of biotic
stress. The work will also revise the most important abiotic stress factors affecting the measurements
as well as practical issues that need to be considered in order to implement this technique, particularly
at the field scale.

Keywords: Remote sensing; proximal sensing; thermography; plant phenotyping





 1. Introduction
Citation: Pineda, M.; Barón, M.; Environmental conditions driven by climate change and infections are great challenges
Pérez-Bueno, M.-L. Thermal Imaging that need to be overcome by modern agriculture. The economic loss in agriculture caused by
for Plant Stress Detection and increasing environmental pressures could reach an annual 0.3% to 0.8% of projected global
Phenotyping . Remote Sens. 2021, 13, gross domestic product by the end of the century [1]. Moreover, plant diseases are the main
68. https://dx.doi.org/10.3390/ cause of the drop in production and economic losses in agriculture worldwide, reaching
rs13010068 yield losses of 20 to 30% depending on the crop [2]. Current practices and social activities
-such as intensified monoculture in large areas, the use of genetically uniform plant varieties
Received: 26 November 2020
and the development of global supply chains and logistic activities- contribute largely to
Accepted: 24 December 2020
the widespread of plant disease epidemics and rapid pathogen evolution [3].
Published: 27 December 2020
Plant phenotyping based on imaging techniques is a pertinent approach to quantify
the appearance and performance of crops under different environmental conditions while
Publisher’s Note: MDPI stays neu-
addressing the spatial heterogeneity of crop fields. Therefore, plant phenotyping, applied
tral with regard to jurisdictional claims
in published maps and institutional
to precision agriculture, is a valuable tool for the diagnosis and detection of plant stress,
affiliations.
even in the absence of symptoms. Optical sensors have been used to study (a) the response
of plants to pathogens, pests and abiotic stressors; (b) to identify primary disease foci; (c) to
monitor resistance or susceptibility of different plant genotypes to specific stress factors;
(d) to evaluate the severity of symptoms; (e) and to assess plant biomass and yield [4].
Copyright: © 2020 by the authors. Li- Stomatal activity is one of the most important physiological traits for plant growth
censee MDPI, Basel, Switzerland. This and development. It plays a crucial role in the carbon and water balance by controlling
article is an open access article distributed photosynthesis and transpiration [5]. Hence, stomatal conductance to water (gs ) is related
under the terms and conditions of the to yield and to the tolerance of environmental stresses [6] and correlates strongly with leaf
Creative Commons Attribution (CC BY)
temperature [7–9]. Thermal long-wave infrared (TIR) cameras (or simply thermal cameras)
license (https://creativecommons.org/
are calibrated sensors able to record emitted radiation in the thermal range (8–14 µm)
licenses/by/4.0/).

Remote Sens. 2021, 13, 68. https://dx.doi.org/10.3390/rs13010068 https://www.mdpi.com/journal/remotesensing

Remote Sens. 2021, 13, 68 2 of 21

and provide images representing temperature values per pixel. Thus, conventional, time-
consuming ground-based gs measurements can be feasibly replaced by thermal images
evaluating plant physiological status at different scales in short periods of time [10,11]. Ad-
ditionally, highly sensitive thermal cameras with a relatively simple operational procedure
have become more available to research groups, at a lower cost and at higher spatial reso-
lution [12,13]. Moreover, TIR imaging is a very valuable method of stress detection prior to
the appearance of symptoms since it operates out of the visual range of the spectrum [14].
However, some considerations must be taken when interpreting thermograms in terms
of gs since plant surface temperature is mainly driven by environmental factors such as
air temperature and relative humidity. Even though high-end thermal cameras carry out
corrections for these two parameters, there are other factors affecting canopy temperatures,
such as wind speed and light intensity, as well as by plant features, ranging from leaf size
or angle to canopy structure. A number of corrections for these factors can be found in
the literature as TIR stress indices (Table 1). Some of these parameters have been found
to correlate with physiological traits related to the water balance status of plants (Table 2).
The most common TIR parameters are:
1. Normalized canopy or leaf temperature with reference to air temperature (∆T), uti-
lized as an index of crop water status. The applications of ∆T was recently reviewed
by Still et al. [15];
2. Crop water stress index (CSWI), which introduces two baselines: (Tcanopy − Tair )wet
as the estimated difference for a well-watered plant, and (Tcanopy − Tair )dry for a
dry (non-transpiring) plant. CWSI is one of the most commonly used normalization
methods for TIR measurements, which overcomes the effects of other environmental
parameters affecting plant temperature [16,17];
3. Index of stomatal conductance (IG ), since it is directly proportional to this parame-
ter [18];
4. Maximum temperature difference (MTD), calculated for every leaf or sample [19].
This parameter has only been correlated with the severity of symptoms for several
diseases, as reviewed in [20,21];
5. Normalized relative canopy temperature (NRCT), based on the maximum and the
minimum temperature measured in the whole field trial. This parameter has been
found to be a valid estimation of the crop water status [22];
6. Average canopy temperature (Tav ), based on maximum and minimum values of
temperature, was one of the first parameters used by the conventional infrared
thermography [23,24]. However, this parameter can excessively simplify outcome
data, and some important thermal information can be lost. Estimated shape factors
derived by fitting the whole temperature data of the thermal images to the Weibull
distribution could solve this constraint [25].

Table 1. Most commonly used thermal long-wave infrared (TIR) parameters.

TIR Stress Index Formula Ref.

∆T, normalized canopy or leaf temperature Tcanopy − Tair or Tleaf − Tair [26]
CWSI, crop water stress index (Tcanopy − Tair )− (Tcanopy − Tair )wet [17,27]
(Tcanopy − Tair )dry − (Tcanopy

− Tair )wet

IG , index of stomatal conductance (T dry −Tleaf [18]

(T leaf −Twet )
MTD, maximum temperature difference Tleaf_maximum −Tleaf_minimum [19]
NRCT, normalized relative canopy temperature Tleaf −Tminimum [22]
Tmaximum −Tminimum
Tmaximum_average −Tminimum_average
Tav , average canopy temperature Tmaximum_average
[24]
Remote Sens. 2021, 13, 68 3 of 21

Table 2. Correlations between TIR stress indices (TIR SI) and physiological parameters (physiol. param.) applied to estimate
physiological traits related to water stress or salinity at proximal (PS) and remote sensing (RS) scales. ∆T, normalized
canopy temperature; AN , net photosynthesis rate; CWC, canopy water content; CWSI, crop water stress index; Em , leaf
transpiration rate; Ψ, hydric potential; gs, stomatal conductance; IG , index of stomatal conductance; NRCT, normalized
relative canopy temperature; RWC, relative water content; SM, soil moisture; Tav , average canopy temperature; Tcanopy ,
canopy temperature; Tleaf , leaf temperature.

TIR SI Physiol. Param. Plant Species Scale Ref.

gs Papaya PS [28]
∆T
Vineyard, corn, olive, citrus, poplar, almond,
RS [29–38]
apple, persimmon
Em Papaya PS [28]
AN Papaya PS [28]
Vineyard, olive, citrus, almond, Prunus sp.,
Ψ RS [29,32–35,38–43]
persimmon, apple

gs Fava bean, spinach PS [44,45]

Vineyard, olive, potato, almond, pistachio RS [29,31,38,46–57]
CWSI Vineyard, Prunus sp., almond, cotton, olive,
Ψ RS [29,38,40,43,48,49,53,55–59]
citrus, pistachio
Em Olive RS [53]
SM Corn PS [60]

gs Fava bean PS [44]

IG Vineyard RS [23,29,38,46,50–52,57]
Ψ Vineyard RS [29,38,57]
RWC Wheat PS [61]
NRCT
CWC Wheat PS [61]
Tav gs Vineyard RS [46]
gs Vineyard, citrus, almond RS [29,52,55,62,63]
Tcanopy Ψ Vineyard, cotton, citrus, almond RS [29,55,63,64]
SM Soybean RS [65]
Tleaf gs Papaya, barley, wheat, rice PS [28,66,67]
Em Papaya PS [28]
AN Papaya PS [28]

Despite the wide use of thermography applied to agronomy, this technique per se
has a very limited capacity for diagnosis. Indeed, temperature raises may be due to
stomatal closure, which is on its own an unspecific mechanism of plant defense against
both abiotic and biotic stressors. Even more, temperature raises can also respond to a
decreased capacity for water evaporation or even to the loss of vegetation [10]. In contrast,
some stresses can cause temporary decreases in leaf temperature. That would be the case
of some pathogens that can interfere in the regulation of stomatal movements to favor
their entry to the mesophyll [68]. As a consequence, alterations in TIR parameters stand
as ambiguous clues for diagnosis. Moreover, abiotic stress factors (mostly drought, soil
salinity or extreme ambient temperature) also cause increases in canopy temperature.
This is most important under natural conditions, where abiotic stressors are difficult to
assess and avoid. Keeping in mind that under such conditions, several stress factors often
affect the vegetation simultaneously, possible misinterpretations of TIR data would lead to
inaccurate determination of the incidence and severity of a particular pathogen infection
or even to a wrong diagnosis.
To overcome the restraints of thermography as a diagnostic technique, authors have
increasingly applied it in combination with other imaging techniques. Roitsch et al. [69]
and Sperschneider [70] reviewed the implementation of TIR cameras with other sensors,
such as RGB, multi- or hyperspectral cameras, in phenotyping platforms. The identification
of spatial and temporal patterns of TIR parameters in combination with other relevant
vegetation indices (VIs) could be of great help to establish robust methods for the early di-
Remote Sens. 2021, 13, 68 4 of 21

agnosis in crop fields. However, a preliminary analysis of a given plant-stressor interaction

is desirable to obtain a stress-specific signature [20].
The use of complementary imaging techniques provides valuable and very complex
information. This complexity is caused by the increasing number of dimensions that can
be considered and the incessant improvements in their spatial and temporal resolution.
To enhance our capacity for data analysis, most recent works have included data-mining
in their analysis. This multidisciplinary approach, based on probability theory, statistics,
decision theory, visualization and optimization, outperforms more conventional statistical
analysis in terms of finding patterns in data [71,72]. Classifiers are algorithms able to learn
patterns from a database of known samples and, based on that knowledge, to identify or
categorize new samples [73]. When applied to agriculture, this approach facilitates the
interpretation of data and the decision-making process to such an extent that no study
appears to be complete without this type of analysis.
Thermography is extensively used for stress detection from lab to field scale by either
proximal or remote sensing (Figure 1). On one hand, proximal sensing (mainly in growth
Remote Sens. 2020, 12, x FOR PEER REVIEW 5 of 21
chambers and greenhouses) refers to imaging single leaves or entire plants from a close
be considered
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Figure 1.
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remote sensing scale.

Physical and technical

Thermography aspectsused
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for stress detection scientific
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by either
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sensing (Figuremethods
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(mainly in growth
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and greenhouses) plant
refers to phenotyping
imaging single[77,78],
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distance to the target. The camera could be mounted on a static stand or small and me-
dium-size robots, including high-throughput platforms. On the other hand, remote sens-
ing refers to measurements taken in open fields with imaging sensors implemented on a
wide range of devices, such as cranes, vehicles, robots and unmanned aerial vehicles
Remote Sens. 2021, 13, 68 5 of 21

Other aspects related to thermography, such as available imaging sensors and evaluation
of their potential [79,80], their use in phenotyping platforms [69,81,82] or UAVs [76,83–85],
and their applications have also deserved special attention by many authors. Moreover,
other TIR applications have also been thoroughly reviewed elsewhere [15,20]. Furthermore,
very recent works reviewed the state of the art in the application of artificial intelligence to
stress detection [70,72]. Despite the vast number of works addressing the use of thermogra-
phy for plant stress detection, little attention has been paid to the physiological perspective
of temperature alterations related to stressed plants. Attending to this need, this review will
revise the most relevant applications of thermography to agriculture with the main aim of
providing TIR camera users with a collection of host plant–pathogen systems described in
the literature in terms of thermal response and the mechanisms of plant defense involved.
Furthermore, a state-of-art review on the detection of abiotic stress by thermography will
complement our current knowledge on thermography applied to the diagnosis of biotic
stress in plants.

2. Biotic Stress Detection by Thermography at Different Scales

Stomata are the main natural entry of pathogens into the plant tissues. Hence, the regu-
lation of the stomatal movements plays a key role in plant defense against microbes [86]. The
recognition of a potential pathogen by plants usually triggers stomatal closure; to counteract
this defense response, some pathogens are able to override the plant signaling pathways to
activate stomatal aperture [87]. Other effects of pathogen infection include disturbances on
leaf development, cell wall and leaf cuticle composition or integrity, alterations in the plant
metabolism or even necrosis of the tissues. These physical and chemical disturbances affect
the plant water status, which can be monitored by thermography [88–90].

2.1. Proximal Sensing on Growth Chambers and Greenhouses

2.1.1. Viral Infections
Even when some virosis cause alterations neither in gs nor in leaf temperature [91],
thermography is very often helpful in tracking viral infections on plants. Most of those
works report temperature increases between +0.5 and +1.5 K; on the contrary, some works
reported decreases in leaf temperature of −0.5 K relative to mock-controls. Hypersensi-
tive response (HR) to Tobacco mosaic virus (TMV) could be visualized as spots of elevated
temperature before any disease symptoms became visible on tobacco leaves. Those spots
were confined to the site of infection as a result of the HR triggered by salicylic acid. On
the other hand, no thermal response was observed on susceptible tobacco-TMV-infected
plants [92]. In the case of Pepper middle mottle virus (PMMoV)-Nicotiana benthamiana plants,
virus spreading through asymptomatic leaves could be first detected by an increase in
temperature on the tissues around the main veins. This effect extended to adjacent tissues
before the spreading of the virus across the midrib of the leaf, as shown by immunolocaliza-
tion. Interestingly, the thermal symptoms caused by the most severe strain of PMMoV were
detected before those caused by the less virulent one [93]. Among other tobamoviruses,
Cucumber mosaic virus (CMV) and Cucumber green mottle mosaic virus (CGMMV) have a
particular impact on cucumber production. Plants infected with CMV displayed homoge-
neously higher temperature in the whole inoculated leaf relative to the controls, whereas
leaves of CGMMV-infected cucumber plants showed a heterogeneous temperature pattern,
consisting of cold spots at the infection sites. However, none of those changes was de-
tectable presymptomatically. Nevertheless, classificatory algorithms could early detect the
infection caused by each pathogen when combining data obtained by TIR, fluorescence and
hyperspectral imaging [94]. Another virus of agricultural interest is the Sweet potato feathery
mottle virus, which is the most widespread virus that infects sweet potato plants, causing
devastating problems when co-infecting with Sweet potato chlorotic stunt virus. Higher leaf
temperatures were associated with more severe symptoms; thus, plants co-infected with
both viruses displayed higher temperatures than single virus-infected plants [95].
Remote Sens. 2021, 13, 68 6 of 21

2.1.2. Bacterial Infections

In the case of bacterial-infected plants, literature reports temperature changes relative
to the controls ranging between −3.3 K and +3 K. The tumor caused by Agrobacterium
tumefaciens in the hypocotyl of castor oil plant produces irreversible disruption of the plant
epidermis and hence, the tumor lacks a protective cuticle against water loss. Moreover,
stomata located at the tumor edge are hypertrophied and non-functional; as a consequence,
the tumor surface was the coldest part of the plant [96]. Some works have studied the
role of plant defense elicitors produced by bacterial pathogens. That is the case of the
proteinaceous harpin synthesized by the bacterium Erwinia amylovora. When infiltrated
in the leaves of Nicotiana sylvestris wild plants, harpin induced a marked presymptomatic
cooling at the inoculation sites, followed by an increase of temperature during the HR [97].
The same trend was described for spots of bacterial canker caused by Pseudomonas syringae
pv. actinidiae on kiwifruit leaves [98]. The decrease in temperature localized at the infection
sites could be related to bacterial virulence factors that actively open the stomata by
interfering with hormonal signaling pathways leading to stomatal closure [99]. On the
other hand, it is well known that recognition of some pathogen-associated molecular
patterns triggers stomatal closure to impede bacterial entrance through these natural
apertures [68]. In bean plants, P. syringae pv. tomato DC3000 induces an HR, whereas
P. syringae pv. phaseolicola 1448A produces systemic infection. First symptoms are evident
after 10 h and 2 days post-infection, respectively. Thermography could presymptomatically
reveal those bacterial challenges as an increase of temperature of the inoculated areas at 1
and 2 h post-infection in the case of HR and systemic infection, respectively [100].
Several works have addressed the effect of the Dickeya dadantii infection on plant tran-
spiration by thermography. This bacterium usually produces soft-rot, a characteristic tissue
maceration, as in the case of N. benthamiana infected at high inoculum dose. After mechani-
cal infiltration, the temperature of the affected areas raised presymptomatically, linked to
an increase in hormones controlling stomatal closure. In subsequent days, the temperature
continued rising, affecting the whole leaf. However, N. benthamiana can activate an efficient
defense response against D. dadantii when the plant is inoculated at doses resembling the
natural infection. In this case, after an initial increase in temperature of the infiltrated
area, infected plants could recover, and temperature subsequently decreased [101]. Inde-
pendently of the inoculum dose, D. dadantii does not cause tissue maceration on melon
leaves. It produces brownish spots at the inoculation sites that evolve chlorosis in the
surrounding tissues in successive days; those symptoms appeared earlier when high dose
concentrations were applied. Only infiltrated areas shown increased temperatures at the
beginning of the infection process when inoculated at a low dose; the whole leaf finally
displaying higher temperature respecting to the controls. However, when a high inoculum
dose was applied, the whole melon leaf displayed a higher temperature [102]. The whole
leaf of another cucurbit, such as zucchini, displayed higher temperature relative to the
controls when inoculated with D. dadantii, whereas visual symptoms (different degrees
of chlorosis proportional to the inoculated dose) were circumscribed to the infiltrated
spots [103,104]. Features extracted from TIR and multicolor fluorescence images were used
to feed algorithms, which provided a good performance of classification of plants into
categories of infected and controls in both melon and zucchini plants [102–104].

2.1.3. Interactions with Pathogenic Fungi and Oomycetes

Thermography has been widely used to assess the effect of fungi and oomycetes on
host plant transpiration. Depending on how these pathogens interact with host plants,
initial phases of pathogenesis can induce increases or decreases in leaf temperatures
affecting only the inoculation sites or wholes leaves. Subsequent symptoms development
may cause transitory drops in temperature as the affected cells die and lose water. Later
infection phases usually lead to an increase in temperature due to the lack of natural
cooling of the necrotic tissues. Concerning healthy areas, it is possible to find in the cited
literature that biotrophic fungi and oomycetes can cause temperature decreases ranging
Remote Sens. 2021, 13, 68 7 of 21

from −0.1 to −2.5 K, whereas increases have been registered from +0.6 to +2 K. For their
part, hemibiotrophic pathogens can decrease leaf temperature between −0.6 and −2.2 K, or
contrary, increase it in +0.4 to +7.5 K. Finally, it is possible to register temperatures decreases
between −2 and −5 K and increases ranging from +0.3 to +9 K when necrotrophic fungi
are studied by TIR imaging.
Concerning infections caused by biotrophic fungi leaves from wheat plants infected
with Blumeria graminis or Puccinia striiformis (fungi causing powdery mildew and stripe
rust, respectively) displayed low temperatures due to the very low resistance to water
evaporation of growing mycelia [105,106]. The phytopathogens Pseudoperonospora cubensis
and Podosphaera xanthii are the causal agents of cucumber downy mildew and cucurbits
powdery mildew, respectively. In cucumber leaves, these pathogens produce infective
spots with lower temperatures than the surrounding healthy areas due to an abnormal
stomatal opening. In the case of P. xanthii infection, the thermographic detection was
not presymptomatic, whereas disease caused by P. cubensis could be revealed one day
before the appearance of symptoms. Under laboratory conditions, the MTD increased
during both pathogenesis and was related to disease severity [19,94,107,108]. Despite
being a biotrophic oomycete, P. cubensis also produces necrosis in the latest infection phase
associated with an increase in cucumber leaf temperature [19,108]. Leaves of rose infected
with the fungus Podosphaera pannosa var. rosae (causal agent of powdery mildew in roses)
showed a presymptomatic decrease in temperature. Furthermore, two algorithms were
trained on features extracted from TIR images, obtaining high accuracy in classifying
healthy and infected plants [109]. Raza et al. [110] also used information extracted from TIR
and RGB pictures to automatically detect tomato plants infected with Oidium neolycopersici
in a presymptomatic way, but the work did not address the physiological changes caused
by the fungus.
Regarding hemibiotrophic fungi, TIR imaging could describe the severity of the
infection, which could be related to the disease stages but also to the host plant resistance
to the pathogen. Thus, Oerke et al. [111] and Belin et al. [112] analyzed apple trees
suffering from apple scab. In that case, the detection of infection, as well as differences
in the virulence of several Venturia inaequalis isolates infecting apple trees, were detected
more accurately by thermography than by chlorophyll fluorescence imaging. The thermal
response was presymptomatic and consisted of spots of decreased temperature due to
the subcuticular growth of V. inaequalis. A soilborne fungus, Rhizoctonia solani, induces
necrosis in lettuce plants, which could be visualized as an increase in leaf temperature
and MTD [113]. The damage produced by another soilborne fungus, Fusarium oxysporum,
to whole cucumber leaves could be detected as a presymptomatic raise in temperature
induced by abscisic acid, followed by a slight decrease as wilt symptoms developed. Finally,
the temperature of whole leaves presenting necrosis increased again [114]. On the contrary,
pea plants infected with this fungus showed an early and slight reduction of temperature
compared to the control plants. At an advanced stage of the infection, the leaf temperature
increased above control levels in the case of susceptible plants, whereas the temperature of
those showing F. oxysporum-resistance remained similar to the controls [115].
In the case of infections caused by necrotrophic fungi, sugar beet plants inoculated
with Cercospora beticola (causal agent of Cercospora leaf spot) displayed spots of presymp-
tomatic low temperature corresponding to the infection sites. Cold spots appeared pro-
gressively until covering the whole leaf surface, whereas lesions were hardly visible by
the naked eye. Toxins influencing cell membrane permeability and produced by C. beticola
could account for this temperature decrease [92]. Aspergillus carbonarius is a fungus causing
sour rot of grape berries and produces ochratoxin-As, toxic for humans. Mycelium growth
areas showed low temperatures that identified affected fruit sites at the very early-stages of
A. carbonarius infection [25]. Thermography also revealed that Alternaria alternata, A. bras-
sicae and A. brassicicola caused a decrease of temperature during the first seven days of
infection on oilseed rape leaves, followed by a temperature increase in successive days.
However, those plants inoculated with A. dauci only developed increases of mean tem-
Remote Sens. 2021, 13, 68 8 of 21

perature at 21 days after inoculation [116]. The infection with Botrytis cinerea (gray mold)
on bean plants caused a presymptomatic increase of temperature at the infection sites. In
subsequent days, leaves developed hot brownish necrotic lesions surrounded by a lower
temperature area [117]. Contrary, B. cinerea–infected roses first showed a decrease of tem-
perature at regions where lesions were initially formed, followed by a rise in temperature
once necrosis occurred [109]. Rosellinia necatrix (soilborne fungus causing white root rot) is
one of the most important constraints to production for a wide range of woody crops such
as avocado. In the late phases of R. necatrix infection, trees undergo a water deficit in the
aerial part due to failure of the root system [118]. As a result, infected plants experienced a
significant increase in leaf temperature from the early symptomatic stage onwards [119].
Furthermore, infected avocado trees in an orchard could be detected by thermography (see
Section 2.2) [120].

2.1.4. Herbivory and Parasitic Plants

Herbivore insects disrupt the integrity of leaves, leading to uncontrolled water loss
from wounds and triggering intricate processes that affect gas exchange also in the re-
maining leaf tissue. Thus, it is possible to find temperature drops from −0.3 to −3 K
in the literature. TIR images of soybean leaflets affected by corn earworm caterpillars
(Helicoverpa zea) showed that leaf areas adjacent to wounds were cooler than distant regions
or sister leaflets [121]. The same leaf temperature pattern was visible after injuries caused
by cabbage looper (Trichoplusia ni) instars on Arabidopsis [122], tobacco hornworm (Man-
duca sexta) on Nicotiana attenuata [123], or larval gypsy moth (Lymantria dyspar) and gall
damage produced by midge flies (Harmandia sp.) on aspen leaves [124]. When elevated
CO2 was applied to the atmosphere, the cooling effect of gall formation on remaining leaf
tissue was reduced [124].
Thermography was also useful in the detection of plants infested by parasites, reveal-
ing temperature increases (from +0.4 to +0.9 K) due to a reduction in the plant water uptake
by affected roots. Examples of these interactions are the nematode Heterodera schachtii
with susceptible sugar beet cultivars [125], as well as the obligatory root parasitic plant
Orobanche cumana (broomrape) and sunflower [126]. The early detection of broomrape
by nondestructive techniques was unprecedented since natural infestation causes subtle
alterations on host physiology and proceeds unnoticed until the emergence of the floral
shoots, by the time of sunflower bloom.

2.2. Remote Sensing on Crop Fields

In crop fields, thermography has facilitated the detailed analysis of crop fields affected
by pathogens, helping in the localization of areas where plants are infected and requiring
urgent intervention [127]. In general, pathogen-infected plants show changes in their
temperature of -2 K to +3.1 K, relative to the temperature of healthy plants; however, it is
worth noticing that these values should be handled with care depending on the sensitivity
and the accuracy of the used TIR cameras. The identification of potentially infected plants
using classifiers provides accuracies ranging between 59 and 89%, depending on the
applied algorithm and parameters used to feed it.
In sugar beet, canopy temperature correlated significantly with the density of the
nematode parasite H. schachtii in the case of a susceptible cultivar, whereas no correlation
could be found for the resistant one [128]. P. syringae pv. actinidiae infection in kiwifruit
orchards was assessed by TIR maps based on canopy temperature. Images revealed
that infected trees were significantly warmer than the healthy ones, being localized in
the outer canes of the canopy [98]. Temperature increases measured on pines infected
with Dothistroma septosporum (causal agent of red band needle blight) and on winter wheat
infected with Zymoseptoria tritici (causing septoria leaf blotch) could be positively correlated
to the damages caused by these hemibiotrophic fungi [90,129]. Necrotic spots on leaves
from three woody trees (oriental cherry, Japanese cornel and sawtooth oak) caused by three
Remote Sens. 2021, 13, 68 9 of 21

fungi (Mycosphaerella cerasella, Elsinoe corni and Tubakia dryina, respectively) can also be
detected as dots with higher temperatures relative to healthy areas [130].
The fusion of thermography with other imaging techniques such as multi- or hyper-
spectral reflectance or chlorophyll fluorescence imaging cameras is very often an adequate
approach for stress detection. The combination with chlorophyll fluorescence imaging al-
lowed monitoring several constraints (fungal infection, galls and chewing damages caused
by arthropods) in understory hardwood saplings. Thus, changes in transpiration could be
related to photosynthesis impairment in affected trees [131]. However, the combination
of TIR imaging with multi- or hyper-spectroscopy reflectance is more feasible since both
techniques are based on passive measurements. Moreover, it is possible to obtain multi-
ple reflectance VIs that could correlate with physiological parameters. Furthermore, VIs,
together with temperature derived parameters, could be implemented on algorithms to
classify plants into categories of interest in the earliest stages of infection. That was the
case of important bacterial diseases causing a high impact on both agriculture and the envi-
ronment, such as citrus greening or Huanglongbing in citrus trees [132], or Xylella fastidiosa,
a quarantine pathogen in olive orchards [133].
In the case of diseases caused by foliar fungal pathogens, the joint use of thermography
and reflectance made it possible to discriminate between severity levels. That was the
case of red leaf blotch (caused by Polystigma amygdalinum) in almond trees [134] and also
early and late leaf spot diseases (caused by Passalora arachidicola S. Hori and Cercosporidium
personatum, respectively) on peanut trees [135]. Minimum temperature corrected by air
temperature showed a negative correlation with the normalized difference vegetation index
(NDVI) in opium poppy orchards infected by the oomycete Peronospora arborescens (causal
agent of downy mildew) [136]. Furthermore, a strong relationship between yield, several
VIs and canopy temperature was observed in maize plants suffering tar spot complex
(caused by Phyllachora maydis and Monographella maydis) [137], as well as in chickpea
infected with Ascochyta rabiei (causing Ascochyta blight disease) [138].
∆T correlated with disease severity caused by soilborne fungal pathogens, such as
Verticillium dahliae (causal agent of Verticillium wilt) in olive trees or R. necatrix in avocado
trees. Moreover, classifying algorithms applied to the data obtained by spectral and TIR
imaging could identify affected trees with high accuracy [120,139,140].

3. Assessing of Plant Abiotic Stress by Thermography

In natural environments, abiotic stress conditions often concur with biotic stresses,
making their evaluation difficult. For this reason, it is important to understand how abiotic
conditions can affect vegetation. The successive sections will review how thermography
has been applied to monitor crop water stress, salinity, nutrient availability, and application
of herbicides, among others, at proximal and remote scales.

3.1. Proximal Sensing on Growth Chambers and Greenhouses

Drought, which importance emerges from the damage caused and its extent, is con-
sequently one of the main abiotic stresses monitored by TIR imaging to help farmers to
establish precise water management and scheduling [141]. Most of the studies related to
drought stress have been conducted in crop fields, but it is possible to find some works
carried out on plants grown under controlled conditions (Table 2). Furthermore, salinity
is essentially water stress that results from the osmotic effect of ions in the soil solution,
reducing the water availability for plants. In addition, ions can accumulate in plant leaves
up to toxic concentrations [142]. Thus, TIR imaging provides an opportunity to screen
for salinity tolerance traits in a reliable, quantitative and efficient manner. The effects of
different abiotic stress factors on leaf temperature at proximal sensing are summarized in
Table 3. The increase in temperature registered in these works for infected plants ranges
from +1.5 to +6 K.
Remote Sens. 2021, 13, 68 10 of 21

Table 3. Effects of several abiotic stress factors on leaf temperature as measured by thermography at proximal sensing scale. Arrows (↑) denote increment in leaf temperature due to the stress condition.

Category Stress Factor Application Plant Effect on Leaf Temperature Ref.

Papaya, spinach, fava bean, corn, wheat, ↑ detected as alterations in TIR
Water Drought Roots [28,44,45,60,61,143,144]
rice, lentil stress indices
Salinity Roots Barley, rice, wheat ↑ proportional to salt concentration [66,67]
Nutrient O2 Roots Cotton ↑ stomatal closure [145]
deficiency Mg Roots Bean ↑ prior to chlorosis [117]
Atmosph. High O3 Leaves Subterranean clover ↑ under long-day conditions [146]
UV-B Leaves Pothos plant, Arabidopsis ↑ under UV-B light [147]
Potato, cranberry, oilseed rape, barley ↑ since ice nucleation is an
Low T Ice nucleation [148–154]
blackcurrant, tomato exothermic process
↑ from vascular tissues towards the
Linuron Roots Bean [155]
leaf edges
Herbicide
Glufosinate Leaves (spray) Bean ↑ gradually [156]
↑ in the spot, expanding to the rest of
Metribuzin Leaves (droplets) Goosefoot [157]
the leaf
Remote Sens. 2021, 13, 68 11 of 21

3.2. Remote Sensing on Crop Fields

Temperature differences ranging from +0.7 to +7 K between healthy and stressed
plants have been reported in the literature at a remote sensing scale. These alterations in
canopy temperature allowed stress detection with accuracies up to 75% using classificatory
algorithms based on TIR stress indices.
Vineyards under different water regimes are proposed as an exemplary study model
thanks to the geometry of orchards. Moreover, climate change threatens the most important
wine-producer countries worldwide, which will suffer increased frequency and severity
of drought periods. On the contrary, fine-tuning irrigation management during the grow-
ing season leads to a slight-to-moderate water deficit, which stimulates optimal grape
quality without significantly compromising yield [47]. Many authors have monitored
physiological parameters related to water balance by handheld devices and correlated
them with stress indices extracted from TIR images (Table 2). They found that TIR imaging
can distinguish between irrigated and non-irrigated canopies and even between different
deficit irrigation treatments. However, the relationship between TIR stress indices and
physiological parameters was found to be stable throughout the season in some cases [47]
or, on the contrary, affected by the phenological stage or the varieties [49,158]. All these
works have used TIR ground-based cameras positioned (lateral or nadir) or implemented
on UAVs. However, it is also possible to use TIR images from Landsat-5 for irrigation
management purposes [159].
As the water demand for agriculture is steadily increasing, exploring indices obtained
by thermography to evaluate drought stress in other crops different from vineyards also
has been extensively addressed (Table 2). The efficiency of the VI named photochemical
reflectance index (PRI) as an indicator of water stress was evaluated by TIR imaging in
olive and peach orchards under different water regimes. It was found that PRI showed a
higher correlation with ∆T and gs than other vegetation indices [30,160]. Regarding the
monitoring of water regimes in crops using satellite images, thermal images taken with
ASTER could distinguish between rain-fed and artificially irrigated olive tree orchards [161].
Based on these works, it can be concluded that thermal information remotely obtained by
TIR cameras, alone or in combination with other imaging techniques, is robust enough to
estimate the water status of crops and to help farmers to establish an appropriate irrigation
scheduling for plantations. However, this conclusion should be taken with caution since
there are exceptions to the rule. As an example, canopy temperature in maize fields under
drought stress only partially reflected gas exchange rates and grain yield, presumably as a
consequence of other alterations caused by this stress factor in plants, such as impairments
in photosynthesis and partitioning rates or alterations in plant leaves and canopy structures
(leading to fluctuations in energy absorption and/or dissipation) [162]. Moreover, the use
of TIR imaging to figure out biologically relevant traits constitutes a challenge under
fluctuating conditions, as recently reviewed by Vialet-Chabrand and Lawson [75].
In addition to physiological variables related to the water status of plants, production
parameters such as grain yield could be evaluated by thermography in cereals. That was
the case of spring barley [163], maize [162] and wheat [61,164,165], where grain yield under
different water regimes showed good correlations with TIR stress indices. CWSI is a good
predictor of garlic bulb biomass under different water availability levels [166]. Another
production parameter, the average fruit weight of mandarins “clementina de Nules” at
harvest, could also be correlated significantly with canopy temperature when different
irrigation regimes were tested [32].
Regarding the nutrient availability in soils, wheat crops growing under higher nitrogen
supplies exhibited lower canopy temperature (and thus, lower CWSI) than those that were
not treated [167]. Kefauver et al. [168] compared different nitrogen treatments in three
barley varieties and elaborated a detailed correlation network of physiological traits, TIR
and other imaging data. Another common stress in crop fields is low temperatures. TIR
imaging has been applied to study frost resistance in apple orchards. When the soil was
Remote Sens. 2021, 13, 68 12 of 21

defrosted, the whole tree froze starting from peripheral twigs, whereas when the soil was
frosted, the tree started to freeze from the trunk at the tree base [169].

4. Future Perspectives
For more sustainable agriculture, the development of tools providing real-time in-
formation on the health status of plants is highly demanded, as well as on their physical
and physiological interactions with their micro- and macro-environment, from soil to
atmosphere. In this sense, the progressive implementation of high-throughput analysis
based on imaging sensors and big data have represented an outstanding innovation [72].
Automation allows rapid evaluations of plants and crops, avoiding subjectivity associ-
ated with visual assessments, reducing the cost of labor and permitting more frequent
assessments on the same plants over time [21]. Indeed, thermography implemented in
high-throughput facilities is contributing to the development of next-generation crops by
crop breeders. However, before thermal sensing is adopted as a routine tool in agriculture
and integrated into decision-making for a wide range of users, further research is necessary
to address current challenges of the technology and interpretation of thermal data [13,76].

4.1. Future Technical Development of Thermography

TIR cameras suffer from challenges common to sensors for image acquisition. At the
proximal sensor scale, the volume of plants that can be monitored at the same time is a
limitation. On the other hand, standardized environments of measurements at a short
distance from the target may complicate the scale up to the field. Indeed, at a remote
sensing scale, atmospheric conditions are challenging. Wind makes the crops move around
or may destabilize UAVs affecting the quality of images. Rain, fog, and other atmospheric
factors could delay scheduled measurements. Even more, satellites could not cover the
entire desired area or do it when atmospheric conditions are inadequate, reducing their
time resolution or even limiting the measurements during long periods in the rainy seasons.
Operational conditions of TIR cameras must be observed, whereas technical features,
such as sensitivity and accuracy, should be taken into consideration when handling thermal
data to avoid misinterpretation of the results. Thermography also needs corrections
to the accuracy of leaf or canopy measurements via the development of more accurate
complementary measurements of atmospheric conditions disturbing the temperature of
the vegetation. That would include wind speed and reflection of solar radiation on canopy
surfaces, dependent on the intensity and quality of light affected by weather conditions
on day flights, as reviewed in [15,80]. Particular attention must be paid to the spatial
and temporal variations in these factors during the actual measurement. Even though
the last generation of thermal cameras can make corrections for relative humidity and
temperature of the air, these atmospheric parameters should be taken into account for other
TIR sensors. These complementary measurements are needed to improve the quality of
the thermal data and to help in interpreting thermal information [15]. The use of current
UAVs minimizes the time-of-measurement effects [76]. On the other hand, flight altitude
affects the measurements due to thermal infrared radiation attenuation by the atmosphere,
requiring some corrections [65]. Focal length, related to the flying altitude, is another
technical feature to take into consideration in airborne thermography [170]. Nonetheless,
nanosatellites and new generation satellites with increasingly higher time and spatial
resolution could be the future of remote sensing applied to agriculture [84].
Public datasets are progressively gaining relevance in plant phenotyping, as in many
other research fields since they offer great opportunities for networking and collaboration.
However, comparing data with other researchers is limited by technical features. A possible
solution for this issue would be the development of a system of standardization (similar to
those issued by the International Commission on Illumination, CIE) that could be adopted
by the international community.
Remote Sens. 2021, 13, 68 13 of 21

4.2. Strategies to Overcome the Intrinsic Non-Specificity of Thermal Patterns

Thermography is a sensitive tool for plant stress detection. However, alterations in leaf
or canopy temperature are intrinsically unspecific for the stressor. Indeed, on crop fields
under natural conditions, plant diseases are often found concurrent with abiotic stresses.
Consequently, in terms of diagnosis, thermography must be used in combination with other
phenomics techniques with the aim of finding distinctive patterns that better explain the
etiology of the disorder, thus helping to cut down potential causes of disease. Appropriate
management and control of abiotic stress factors considering the heterogeneities of the
farmed land appear mandatory to avoid misinterpretations of the thermal imagery. For
example, in orchards, water management can be improved by precise measurements of
soil humidity by thermography, as reviewed by [171]. Thus, an accurate diagnosis and
quantification of the extent and severity of disease-related symptoms can only be achieved
based on a collection of inputs such as the geological features and history of the farmed
land or weather conditions at the time of image collection.
Deep learning is key in the process of turning data into knowledge, particularly when
thermography is integrated with other imaging techniques in a multidimensional analysis,
as recently reviewed by [72]. Public accessibility and interoperability of datasets, from
high-throughput phenotyping platforms and satellites, promoted by cooperative initiatives
such as those funded by the International Plant Phenotyping Network (https://www.plant-
phenotyping.org), are contributing to develop the potential of plant phenotyping [172].

4.3. Uses of Plant Thermography for Agriculture in the Near Future

In recent years, huge investments have been made in plant phenotyping facilities to
support basic and applied research. Further work is needed to widen our knowledge on
plant physiology upon stress as well as developing improved stress detection methods.
Future research should also address the development of more general stress detection
methods, valid for a range of plant species and growth conditions, including location,
or even independent from those factors. The contribution of thermography to precision
agriculture should not be limited to the detection of stress.
Thermography also appears as a very convenient tool to study other aspects of plants
that are out of the scope of this review, such as seeds vigor [173], investigations on circadian
rhythms [174,175], the effects of microgravity on plant physiology [176], interactions with
plant-symbiotic microorganisms [177–180], the impact of climate change in ecology [15],
or food industry [181]. Thermography is also a very relevant tool for screening for mu-
tants [182,183] and cultivars [21] with desirable phenotypes such as pathogen resistance
or improved performance upon certain abiotic stress conditions. In summary, thermog-
raphy implemented in high-throughput facilities is contributing to the development of
next-generation crops by crop breeders.

5. Concluding Remarks
The huge collection of works applying thermography to plants and crops shows that
this technique is overcoming inherent constraints, being able to determine plant water
status and to detect plant stress in a robust, reliable, low-cost way. On one hand, TIR stress
indices are often more reliable than actual temperature values as they counteract the effects
of ambient conditions on the measurement, providing good correlations with physiological
parameters related to the plant water status. On the other hand, the combined use of
thermography with other imaging sensors and the application of big data tools are an
advantageous approach that allows identifying stressed plants and even evaluating the
severity of symptoms. In spite of this, more detailed studies are needed to build a solid
base of knowledge applicable to practitioners. Additionally, platforms based on imaging
technologies should be developed to cover the needs of a wide range of end-users.
Remote Sens. 2021, 13, 68 14 of 21

Author Contributions: Conceptualization, M.P., M.-L.P.-B. and M.B.; investigation, resources, M.P.;
writing—original draft preparation, M.P. and M.-L.P.-B.; writing—review and editing, M.P., M.-L.P.-B.
and M.B.; project administration, M.B.; funding acquisition, M.B. All authors have read and agreed
to the published version of the manuscript.
Funding: This research was funded by Junta de Andalucía, grant number P12-AGR-0370, and
Ministerio de Ciencia, Innovación y Universidades (MCIU) by Agencia Estatal de Investigación (AEI)
and European Regional Development Fund (ERDF), grant number RTI2018-094652-B-I00.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or
in the decision to publish the results.

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