Eur J Plant Pathol (2012) 133:197–209

DOI 10.1007/s10658-011-9878-z

Recent advances in sensing plant diseases

for precision crop protection
Anne-Katrin Mahlein & Erich-Christian Oerke &
Ulrike Steiner & Heinz-Wilhelm Dehne

Accepted: 8 September 2011

# KNPV 2011

Abstract Near-range and remote sensing techniques Keywords Precision crop protection . Plant disease
have demonstrated a high potential in detecting detection . Optical sensors . Hyperspectral techniques .
diseases and in monitoring crop stands for sub-areas Spectral signatures . Thermography
with infected plants. The occurrence of plant diseases
depends on specific environmental and epidemiolog- Abbreviations
ical factors; diseases, therefore, often have a patchy GIS Geographic Information System
distribution in the field. This review outlines recent VIS Visible Region
insights in the use of non-invasive optical sensors for NIR Near Infrared
the detection, identification and quantification of plant SWIR Shortwave Infrared
diseases on different scales. Most promising sensor TIR Thermal Infrared
types are thermography, chlorophyll fluorescence and SVI Spectral Vegetation Index
hyperspectral sensors. For the detection and monitor- PCA Principle Component Analysis
ing of plant disease, imaging systems are preferable to SAM Spectral Angle Mapper
non-imaging systems. Differences and key benefits of ANN Artificial Neural Networks
these techniques are outlined. To utilise the full SVM Support Vector Machines
potential of these highly sophisticated, innovative
technologies and high dimensional, complex data for
precision crop protection, a multi-disciplinary ap-
proach—including plant pathology, engineering, and Introduction
informatics—is required. Besides precision crop
protection, plant phenotyping for resistance breeding The worldwide demand for agricultural products
or fungicide screening can be optimized by these exceeds the supply; hence there is a need to manage
innovative technologies. the worldwide production of agricultural commodities
more efficiently (Von Witzke et al. 2008). Without the
use of new technologies, it will be not feasible to
A.-K. Mahlein (*) : E.-C. Oerke : U. Steiner : work against this trend. The potential yield of
H.-W. Dehne agricultural and horticultural crops worldwide is
Institute of Crop Science and Resource Conservation affected by various kinds of pests and abiotic stress
(INRES)—Phytomedicine, University of Bonn,
factors (e.g. pathogens, insects, weed, nutrition
Nussallee 9,
53115 Bonn, Germany deficiencies or drought stress) which can reduce the
e-mail: amahlein@uni-bonn.de quantity and quality of crop production. Oerke and
198
Dehne (2004) estimated that, without control, dis-
eases, animal pests and weeds may reduce worldwide
crop production by 18, 18 and 32%, respectively;
despite the current crop protection practices, actual
losses to diseases due to fungi, bacteria and viruses
were estimated to be 13% of production potential.
The incidence of pests impairing plant growth in
the field is often rather heterogeneous in time and
space—at least in early stages (Waggoner and Aylor
2000). This variation is due to environmental con-
ditions like edaphic factors, (micro-) climatic con-
ditions and especially due to biological as well as
epidemic specificities of different pests. As the
assessment of this variability in pest incidence is
often hard, and traditional agricultural management
practices assume parameters in crop fields to be
homogeneous, the input of pesticides and manage-
ment actions often does not match actual demands
(Steiner et al. 2008). Considering that the occurrence
of disease depends on specific environmental factors
and that diseases often exhibit a patchy distribution in
field, near-range and remote sensing techniques could
be useful in detecting diseases and in the monitoring
of crops for sub-areas with infected plants. Based on
the information from different sensors and by the
use of geographic information systems (GIS),
application maps can be generated, to manage
agricultural fields with due consideration of spatio-
temporal heterogeneities of diseases (Hillnhütter
and Mahlein 2008). Site-specific application of
pesticides, according to precision agriculture strate-
gies, has the potential to reduce pesticide use, and
thus may cut the economical expenses and ecolog-
ical impacts in agricultural crop production systems
(Gebbers and Adamchuk 2010).
Reliable, precise and accurate estimates of diseases
are important for predicting yield loss, monitoring and
forecasting epidemics and for understanding funda-
mental biological processes (Bock et al. 2010).
Several kinds of innovative sensors have been tested
for their suitability to detect early changes in plant
physiology due to biotic and abiotic stresses. Ther-
mography, reflectance and fluorescence measure-
ments are currently the most promising techniques
(Chaerle and Van der Straeten 2000). In combination
with powerful data analysis methods, these techniques
will be of essential support for further Integrated Pest
Management (IPM) programs for sustainable crop
production.
Eur J Plant Pathol (2012) 133:197–209
For sensory detection of biotic and abiotic stress
factors the sensitivity and the specificity of the signal/
techniques are crucial, in particular for the detection
of plant diseases caused by microorganisms. The
differentiation among diseases occurring on a crop is
an essential feature for operational systems, and,
moreover, the detection of host plant colonization by
pathogens may become feasible even before the
appearance of typical disease symptoms. The unique-
ness of spectral signatures of plant diseases is
controversially discussed in the literature (Nutter et
al. 2010). Stress causing agents, and likewise various
pathogens often cause similar (disease) symptoms and
changes in plant physiology (Nutter et al. 2010;
Stafford 2000). As primary and secondary effects of
different diseases on plant metabolism vary, different
sensor signals should be suitable for the identification
of diseases. However, chlorosis and reductions in
chlorophyll content are caused not only by plant
pathogens, but also by abiotic factors. Therefore,
detailed understanding of plant physiological process-
es related to specific diseases as well as knowledge on
complex interactions between environmental condi-
tions and plants during sensor application is indis-
pensable. A multi-disciplinary approach is essential to
tap the full potential of these highly sophisticated,
innovative technologies and high dimensional, com-
plex data for precision crop protection. Using the
expertise from phytopathology, geography, computer
science and data mining, a new understanding of crop
protection will be formed.
Precision crop protection as a part of precision
agriculture
The use of innovative technologies summarized as
‘Precision Agriculture’ is a promising approach to
optimize agricultural production of crops. In crop
production precision agriculture methodologies are
applied for the site-specific application of fertilizer or
pesticides, automatic guidance of agricultural
vehicles, product traceability, on-farm research and
management of production systems (Gebbers and
Adamchuk 2010). Recently, precision agriculture also
enhanced management decisions in livestock produc-
tion, pasture management, viticulture and horticulture
(Schellberg et al. 2009; Gebbers and Adamchuk
2010). Precision crop production aims to match
Eur J Plant Pathol (2012) 133:197–209
agricultural input and practices to the spatial and
temporal variability within a field, instead of manag-
ing an entire field based on a hypothetical average.
Small-scale site-specific differences can lead to
considerable differences in yield and quality, thus a
better use of resources to preserve the quality and
quantity of agricultural products with respect to
environmental resources is essential (Gebbers and
Adamchuk 2010). The philosophy behind precision
agriculture not only includes a direct economic
optimization of agricultural production, it also stands
for a reduction of harmful outputs into the environ-
ment and non-target organisms. Although overall
levels are below acceptable threshold levels in most
regions, the pesticide residues in water, soil and food
resources have to be minimized in crop production
(Bongiovanni and Lowenberg-Deboer 2004). High
control costs and the environmental impact of
fungicides result in a high interest in site-specific
application according to precision farming techniques,
i.e. monitor and manage spatially-variable fields in a
site-specific manner (Stafford 2000).
Precision disease control is a demanding challenge
within precision agriculture and offers great potential
to reduce the costs and environmental impact of
fungicide use. According to the characteristics of
plant pathogens, site-specific disease management
requires a high density of spatial and temporal
information with regard to the status of any crop
growth-relevant parameter. Disease monitoring and
decision support systems form the basis for site-
specific management of crops showing spatial and
temporal variability in disease incidence and severity
(Steiner et al. 2008). Currently two different
approaches for site specific fungicide application are
under examination; (i) indirect decision-making by
assessing canopy density or crop growth stage
(Scotford and Miller 2005), and (ii) direct detection
of disease or inoculum (West et al. 2010). The first
method largely depends on a mechanical sensor
measuring the resistance of the crop stand to a
pendulum moving through the crop and aims to
adjust the spray volume to crop density in order to
adjust the fungicide concentration per plant biomass
(Dammer 2010). The detection, identification and
quantification of diseases are closely related to
innovative technologies like hyper- and multispectral
sensors or thermography for near-range and remote
sensing. Real-time decision based on the information
199
of a sensing system can control cultural practices
(Stafford 2000). Precise, reproducible and time-saving
methods for disease monitoring—detection, identifi-
cation, quantification—are essential (Bock et al.
2010; Hillnhütter and Mahlein 2008; Steddom et al.
2005). Remote sensing technologies may provide an
alternative to visual disease assessment (Nutter et al.
2010).
West et al. (2003) gave a detailed overview on
sensor-based detection of stress. The nature of the
phenomenon of interest and its environments define
the sensor specifications required (e.g. spatial and
spectral resolution; temporal availability). The poten-
tial of remote sensing techniques for agriculture has
been demonstrated several times (i.e. Franke and
Menz 2007; Galvao et al. 2009; Oppelt and Mauser
2004; Thenkabail et al. 2000); Hillnhütter et al.
(2011a, b); Mahlein et al. (2010); Moshou et al.
(2004) and Steddom et al. (2005) have proven the
potential of spectral sensor systems for the detection
of fungal diseases.
Current research on precision crop protection
focuses on the development of sensors for near–range
(proximal) sensing of crops and diseases in real time.
Integration of different sensor techniques and image
analysis in combination with global positioning will
be an essential step towards online applications.
Sensors—innovations and limitations
Innovative sensor systems can provide detailed and
highly resolved information on crop systems and single
plants. Various non-invasive sensor types can assess
different parameters of the targeted objects, depending
on signal-object interactions. Sensors can be grouped
depending on the measuring range in the electromag-
netic spectrum (visible=VIS, near infrared=NIR, short
wave infrared=SWIR, thermal infrared=TIR), the
measuring scale (near-range or remote), and into
imaging and non-imaging sensors. Sensors may be also
differentiated into (i) passive sensors, i.e. sensors
measuring the characteristic radiation of an object
(thermography) or the reflectance of solar radiation;
and (ii) active sensors, i.e. systems equipped with an
own source of radiation (reflectance, radar, laser,
fluorescence); their detectors record the modifications
of the radiation due to its interactions with the object.
Techniques like thermography may be used in a passive
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as well as in an active mode. Active sensors are less
affected by environmental factors. Chaerle and Van der
Straeten (2000) and West et al. (2003, 2010) gave
detailed overviews on various sensor types used for
assessing plant physiological parameters. Encouraging
approaches are measurements based on thermal char-
acteristics (Jones and Schofield 2008; Lenthe et al.
2007; Oerke et al. 2006), chlorophyll fluorescence
(Chaerle et al. 2007; Rascher et al. 2000) and
reflectance of plants (Oppelt and Mauser 2004;
Peñuelas and Filella 1998; Ustin et al. 2009).
Thermography
Thermography allows the imaging of differences in
surface temperature of leaves, plants or crop canopies.
The emitted infrared radiation in the TIR from 8–
12 μm can be detected by thermographic cameras and
illustrated in false colour images. Each image pixel is
related to a temperature value of the measured object
(s). The performance of thermographic cameras is
characterised by the thermal sensitivity (thermal
range, measurement precision), image resolution
(image pixel size, number of image pixels, depth of
focus), and scan speed (Oerke and Steiner 2010).
Thermography can be applied in terms of near or
remote sensing, from microscope application over
ground-based equipment to airborne sensors. The
major advantage of infrared thermal imaging is the
non-invasive, non-contact, and non-destructive nature
of the technique to determine the temperature distri-
bution of any object in a short period of time
(Vadivambal and Jayas 2011).
Infrared thermography is highly suitable for the
detection of disease-induced modifications in plant
transpiration and water status. Temperature of plant
leaves is determined by temperature of the environment
and plant transpiration rate; leaf temperature increases as
transpiration rate decreases (Chaerle and van der
Straeten 2000; Jones and Schofield 2008; Oerke and
Steiner 2010). Similar to abiotic factors, pathogens
may affect the status of stomata regulating the water
loss of plants. The thermographic method commonly
used in disease detection is the passive measurement of
tissue temperature as determined by the amount of
water transpired, without using any external tempera-
ture influences (Oerke and Steiner 2010). Spatial and
temporal pattern of and within-tissue heterogeneities in
transpiration due to plant diseases can be imaged and
Eur J Plant Pathol (2012) 133:197–209
monitored pre-symptomatically and during further
disease development on different scales.
Local temperature changes due to plant pathogens
or defence mechanisms have been reported by several
research groups. Chaerle et al. (2007) imaged the
hypersensitive response (HR) and developing cell
death induced by tobacco mosaic virus (TMV) and
Cercospora beticola in thermographic studies under
controlled conditions. TMV infection of tobacco
leaves resulted in an initial increase of leaf tissue
due to the accumulation of salicylic acid, whereas
infection of sugar beet leaves by Cercospora beticola
showed rapidly spreading cold spots (Chaerle et al.
2007). Pre-symptomatic thermographic detection of
cucumber downy mildew caused by Pseudoperono-
spora cubensis was reported by Lindenthal et al.
(2005) and Oerke et al. (2006). Depending on the
stage of pathogenesis and the appearance of chlorosis
and necrosis, infection resulted in typical spatial and
temporal temperature patterns. Stoll et al. (2008)
found characteristic thermal responses of grapevine
leaves infected with Plasmopara viticola, before
visible symptoms appeared. For scab infected apple
leaves, differences in disease severity, resistance of
host tissue, and differences in the aggressiveness of V.
inaequalis isolates could be monitored by digital
infrared thermography (Oerke et al. 2011; Fig. 1).
On the field scale thermography may be used for a
direct detection of primary disease foci or diseased
plant parts and for measurements of environmental
conditions favourable for infections by phytopatho-
gens, e.g. leaf wetness and the duration of wetness
periods, to be used in models quantifying disease
risks (Lindenthal 2005). Lenthe et al. (2007) exam-
ined the microclimate of wheat canopies and the
spatial and temporal dynamics of fungal diseases.
First results for a direct detection of disease symptoms
caused by Fusarium head blight on ears of winter
wheat using infrared thermography display significant
higher temperature of infected ears compared to
uninfected ears (Oerke and Steiner 2010). Using this
methodology a target-orientated sampling and site
specific harvesting could be implemented in order to
reduce the health risk from mycotoxins produced by
Fusarium ssp. (Fig. 2).
On the field level, thermography is a promising
tool to monitor spatial heterogeneity in the incidence
of soil-borne pathogens. A patchy occurrence of
above-ground symptoms and low mobility in the field
Eur J Plant Pathol (2012) 133:197–209 201
Fig. 1 Effect of developing
scab lesions caused by Ven-
turia inaequalis on spatial
heterogeneity in leaf tem-
perature of apple leaves.
First thermal effects became
detectable 6 days after in-
oculation. RGB image (a),
thermogram with transects
(b), temperature profiles of
transects through scab
lesions (c)

are characteristic for these pathogens (Hillnhütter et
al. 2011a). Patches of sugar beet infested by Hetero-
dera schachtii with obvious temperature differences
could be detected using aerial thermographic images
(Schmitz et al. 2004). Airborne thermography has
been shown to be useful for the delineation of
management zones within fields—based on the
transpiration of crop canopies related to plant bio-
mass—as well as for the assessment of plant vigour
related to crop yield in fungicide trails (Lenthe 2006;
Stenzel et al. 2007).
As thermography is highly sensitive to environmen-
tal conditions during measurements, practical use of
thermography in precision disease control is limited.
Furthermore, the thermal response (= changes in
transpiration) of plants largely lacks diagnostic potential
for the identification of plant diseases. More sophisti-
cated sensor systems have to be developed or so-called
sensor fusion, i.e. the combination of information from
various sensor systems, may improve the detection
ability (Chaerle et al. 2007; Jones and Schofield 2008).
Fluorescence measurements
Various parameters of the fluorescence of chlorophyll
and other plant metabolites, e.g. phenols, induced by
various light sources (sunlight, laser, etc.) may be
recorded under controlled conditions as well as in the
field. The instruments commonly are active sensor
systems; the technology may be used to assess the
nitrogen demand of crops in the field (e.g. Thoren and
Schmidhalter 2009). As pathogen attack affects also
the photosynthetic apparatus of crops—pigments,
electron transport chain, enzymes of the Calvin cycle
catalyzing CO2 fixation—chlorophyll fluorescence is
modified in many crops (see e.g. Kuckenberg et al.
202
Fig. 2 Detection of Fusarium head scab infected ears in winter wheat at GS 77–79. RGB image (a), thermogram with broad (b) and
narrow temperature range (c) (modified from Oerke and Steiner 2010)
2009; Bürling et al. 2011). Since modifications in
photosynthesis due to the activity of plant pathogens
on the cellular and tissue level lack diagnostic
potential, as with tissue transpiration, measurements
of chlorophyll fluorescence and blue light-induced
fluorescence techniques are not discussed in more
detail. These methods may be very sensitive in the
detection of abnormalities in photosynthesis—see e.g.
reviews by Scholes and Rolfe (2009) and Chaerle et
al. (2009) as well as Csefalvay et al. (2009)—the use
of these active sensors in the field, however, is also
limited by the response time, i.e. the time between
emission and detection of the measuring beam,
restricting the use for on-the-move sensing.
Hyperspectral techniques
The evolution of spectral sensors started with multispec-
tral sensors, to hyperspectral sensors, and to forthcoming
ultraspectral sensors. These technical complex devices
provide a multiplicity of information over the covered
spectral range (350–2500 nm). Spectral resolution of
modern instruments may be <1 nm.
Currently reflectance sensors are classified depend-
ing on their spatial scale, spectral resolution, and the
type of detector, i.e. imaging or non-imaging sensor
systems (Steiner et al. 2008). Airborne or space-borne
far-range systems have lower spatial resolution than
near-range systems and are hardly suitable for the
detection of disease symptoms on the leaf or plant
Eur J Plant Pathol (2012) 133:197–209
scale. The maximal spatial resolution is defined by the
minimum size of a pixel and hence the smallest
identifiable symptom or structure. Technological
advances in sensor development, in particular prog-
ress from multispectral broadband sensors to hyper-
spectral narrowband sensors have drastically
increased the quantity and quality of available
information. Non-imaging sensors average the reflec-
tance over an area depending on the sensor’s field of
view; the mixed information from different objects
hardly allows significant inferences on the reflectance
sources/objects (Mahlein et al. 2010; Steiner et al.
2008). In contrast, cutting-edge hyperspectral cameras
facilitate the detection of both spectral and spatial
information of an object (Fig. 3). The information of a
hyperspectral image is based on the spatial X- and Y-
axes and a spectral Z-axis, which allows a more
detailed and allocated interpretation of the signal
object interaction. Each spatially located pixel of an
image contains the full wavelength information. The
use of innovative hyperspectral imaging systems in
plant pathology and in disease severity assessment is
still in the research stage (Bock et al. 2010).
Mewes et al. (2011) stated that the entire spectrum
from 350 to 2500 nm is not needed to detect crop
stress due to fungal infections. Since narrow spectral
bands are highly correlated to each other, redundant
information is measured. Depending on the object and
aim, just few regions of the spectral range may be of
interest.
Eur J Plant Pathol (2012) 133:197–209
Fig. 3 Structure of hyperspectral image data cube of a sugar
beet leaf with spatial dimensions X and Y and spectral
dimension Z disolaying the continuous spectrum with 210
reflectance values for each pixel of the image
Spectral signature of plant diseases
Leaf reflectance of sunlight in the visible (VIS,
400 to 700 nm), near infrared (NIR, 700 to
1100 nm) and short wave infrared (SWIR, 1100
to 2500 nm) are driven by multiple interactions:
radiant energy absorption induced by leaf chemistry,
scattering of light as a result of leaf surface and internal
cellular structures and radiant energy absorption in-
duced by leaf water content, proteins or carbon content
(Jacquemoud and Ustin 2001).
Hyperspectral imaging and non-imaging sensors
have been proved to be useful tools to detect changes
in plant vigour (West et al. 2010). Changes in
reflectance result from modifications of biophysical
and biochemical characteristics of plant tissue. Dis-
eases may cause modifications in tissue colour and
leaf shape, transpiration rate, crop canopy morpholo-
gy and density as well as variation in the interaction
of solar radiation with plants (West et al. 2010). They
result in modified optical properties of leaf tissue.
Reflectance of leaves is sensitive to plant stress due to
changes in pigmentation, hypersensitive reaction and
cell wall degradation (Blackburn 2007; Chaerle et al.
2007; Carter and Knapp 2001). Disease-specific
symptoms, e.g. succession of chlorotic and necrotic
tissue varying in optical characteristics as well as in
composition, and typical fungal structures like pow-
203
dery mildews, rusts, and downy mildews may be also
detectable.
Composition and content of leaf pigments change
when plants are exposed to pathogens that induce
chlorotic and necrotic symptoms. The pattern of
responses and the degree of up- and down-regulation
of physiological processes are related to the type of
the host-pathogen relationship. Necrotrophs rapidly
kill plant cells and subsequently feed on the nutrients
released from the dead tissue, biotroph pathogens
form haustoria to take up nutrients from living cells.
As characteristic symptoms also differ, different
wavebands may be suitable for the detection of
different diseases. The identification of a disease, its
discrimination from other diseases and abiotic stres-
sors, using sensing techniques is still a challenge in
vegetation monitoring. Interpretation of spectral re-
flectance data without knowledge on spectral charac-
teristics of leaves and typical symptoms is impossible
at present. The best results for the detection of
diseases were obtained in the VIS and NIR range of
the spectrum. Spectral signatures of sugar beet leaves
under the effect of the three diseases Cercospora leaf
spot, powdery mildew and sugar beet rest were
significantly different and disease specific (Mahlein
et al. 2010; Fig. 4). The causal relationship between
diseases and specific spectral changes was stressed
by their dependence on the severity of diseases.
Other researchers successfully used spectral data to
detect Magnaporthe grisea on rice (Kobayashi et al.
2001), Phytophthora infestans on tomato (Zhang et
al. 2003), and Venturia inaequalis on apple trees
(Delalieux et al. 2007). Damage to crops caused by
virus diseases (Naidu et al. 2009) or insects (Carrol
et al. 2008) could also be detected using spectral
sensors.
Since non-imaging hyperspectroscopy has been
used in most of the studies published up to now, the
application of hyperspectral imaging focusing on
spectral information of disease symptoms is limited.
Bravo et al. (2003) used in-field spectral images for
an early detection of yellow rust infecting wheat,
Hillnhütter et al. (2011b) successfully discriminated
symptoms caused by H. schachtii and Rhizoctonia
solani on sugar beet. At the present time, hyper-
spectral imaging is more widespread in the field of
monitoring fruit security and quality. Quin et al.
(2009) developed a hyperspectral imaging approach
to detect canker lesions on citrus fruits.
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Fig. 4 Spectral reflectance of healthy sugar beet leaves and
leaves affected by Cercospora leaf spot, powdery mildew and
sugar beet rust in VIS, NIR, and SWIR. Reflectance was
measured 14 days after inoculation using an ASD-Field Spec
JR (Analytic Spectral Devices (ASD), Boulder, USA)
Analysis of sensor data for disease detection
Powerful methods of data analysis are crucial in the
use of optical sensors for the detection, differentiation
and quantification of plant diseases. Characteristic for
imaging sensor systems, especially of hyperspectral
systems, is the recording of large amounts of
information on the object acquired at the same time.
Since large amounts of data also imply enormous file
sizes and computing times, the analysis of hyper-
spectral data is a complex domain, and different
approaches can be used to obtain satisfactory results.
In thermography, absolute temperature, temperature
differences between leaf tissue and air temperature, or
maximal temperature differences (MTD) of plant
tissue are effective parameters (Oerke et al. 2006;
Oerke and Steiner 2010). The visualisation of
isotherms can be convenient as well to accentuate
hot and cold spots due to infections by leaf pathogens
(Oerke et al. 2011). An interesting approach from
medicine might be adaptable to thermography in
phytopathology; Boquete et al. (2010) used indepen-
dent component analysis for an automated detection
of high tumour risk area in cancer research. An
automated detection of temperature anomalies, indi-
cating zones of diseased tissue with high accuracy has
high potential for future applications like early
detection screening.
Modifications in spectral reflection and differences
between spectral signatures can be distinguished by
calculating difference spectra, ratios or derivations
Eur J Plant Pathol (2012) 133:197–209
(Carter and Knapp 2001; Pietrzykowski et al. 2006).
This methodology is a useful tool to compare spectra
of healthy and diseased plants. Mahlein et al. (2010)
identified different significant regions of difference
spectra from healthy plants and plants diseased with
Cercospora leaf spot, powdery mildew and sugar beet
rust. Based on the understanding of reflectance
characteristics, spectral algorithms, using specific
wavelengths of spectral signatures, have been devel-
oped in remote sensing of vegetation (Blackburn
2007; Thenkabail et al. 2000). They are correlated to
several biochemical and biophysical plant parameters
indicating plant health or vigour. Spectral vegetation
indices (SVIs) are widely used for monitoring,
analysing, and mapping temporal and spatial variation
in vegetation. By calculating ratios of several bands at
different ranges of the spectrum, SVIs result in a
reduction of data dimension, which may be also
useful in effective data analysis for disease discrim-
ination. As pigment concentrations provide informa-
tion on the physiological state of leaves, pigment-
specific SVIs are likely to be useful in the detection of
stresses caused by fungal diseases (Fig. 5). Delalieux
et al. (2007) used SVIs for the assessment of apple
scab due to V. inaequalis at different stages of disease
development. Steddom et al. (2005) calculated SVIs
from multispectral data of sugar beet fields and
compared these indices to disease severity visually
rated by plant pathologists. The use of combinations
of two or more indices improved the discrimination of
three diseases of sugar beet (Mahlein et al. 2010). In a
further approach these SVIs have been used as
features for an automatic discrimination by Rumpf et
al. (2010). Since SVIs commonly used in remote
sensing of vegetation are hardly disease-specific, the
development of disease-specific indices could im-
prove the usefulness of spectral indices for disease
detection.
In remote sensing applications, many classification
and change detection techniques have been developed in
order to obtain maximal information from hyperspectral
data and images. Classification is a procedure of
assigning a spectral signature to a characteristic group
or class, and discriminates these groups from each other.
The classes can be predefined (supervised classification)
or non-predefined (unsupervised classification). Since
disease epidemics and symptom development cause
temporal and spatial changes in crop reflectance, most
classification techniques from remote sensing are likely
Eur J Plant Pathol (2012) 133:197–209
Fig. 5 Spatial illustration of the Normalized Vegetation Index
(NDVI) calculated on hyperspectral imaging data of healthy
sugar beet canopy (a, b) and powdery mildew diseased sugar
to be useful for the detection of disease-induced spectral
changes. Principal component analysis (PCA), spectral
angle mapper (SAM) and machine learning methods like
artificial neural networks (ANN) or support vector
machines (SVM) are the most common methods used
for data analysis (Bauriegel et al. 2011; Zhang et al.
2003; Moshou et al. 2004; Rumpf et al. 2010). The
SAM, calculating the angular difference between an
unknown spectrum and a reference spectrum in an n-
dimensional space has shown high overall accuracies
for the classification of sugar beet diseases (Mahlein
unpublished; Fig. 6).
Moshou et al. (2004) used ANNs to classify healthy
from diseased wheat plants. Rumpf et al. (2010)
successfully differentiated foliar diseases of sugar beet
in a pre-symptomatic stage using SVMs. Quin et al.
(2009) differentiated healthy citrus fruits, canker-
diseased and damaged fruits with a spectral information
based algorithm, yielding in a classification accuracy of
96%. Data mining techniques have been shown to be
superior in distinguishing between more than one type
of stress and different diseases (Moshou et al. 2004;
205
beet canopy. (c, d). High NDVI-values denote vital leaf tissue
(green), low NDVI-values diseased leaf tissue (red-purple)
Rumpf et al. 2010). Implementing these different
algorithms in an interdisciplinary approach, the multi-
dimensional problem of detecting, differentiating and
quantifying various diseases will be solved, marking a
breakthrough in automatic, reproducible, and non-
invasive disease detection. Although all these algorithms
have their own specifications and merits, there is not a
single approach which is optimal for all applications.
All common classification techniques analyze hyper-
spectral images without incorporating information from
spatially adjacent data (Plaza et al. 2009). Simultaneous
multidimensional data analyses of spatial and spectral
patterns may be of high relevance in future, especially
for the interpretation of hyperspectral images for
detection of characteristic disease symptoms.
Fields of application for disease sensing
Optical sensor technologies may be implemented for
precise and successful control of plant diseases in
different fields, e.g. resistance breeding in the field
206
Fig. 6 Automatic classification of Cercospora leaf spot using
spectral angle mapper (SAM) algorithm 14 days after inoculation.
RGB-image of a Cercospora leaf spot diseased sugar beet leaf (a),
grey-scale rule image for healthy tissue where dark pixel belong to
the class ‘healthy’ (b), and false-colour image of the SAM
classification for the classes ‘healthy’ (green), ‘margin’ (red), and
‘necrotic’ (c)
and under controlled conditions, screening of new
fungicidal compounds, precision disease control in
the field. Near-range imaging sensor systems and
Eur J Plant Pathol (2012) 133:197–209
spectroradiometry may be also used in plant pathol-
ogy for investigating the effect of pathogenesis on the
cellular level. Hyperspectral imaging microscopy may
result in new spatial information on structural and
chemical modifications of the plant tissue in the
course of host-pathogen interactions.
Innovative sensor techniques may be applied in
large-scale plant breeding experiments to speed up
screening assays in resistance breeding (Montes et
al. 2007). Plants are commonly inoculated with a
pathogen at a well-known spore concentration and
time. These are optimal conditions for an automatic
hyperspectral screening system with high sensitivity
and specificity. Analogue operations and require-
ments are characteristic for fungicide screening.
Since the identification of diseases is not required
in inoculation experiments, thermography and fluo-
rescence techniques also seem to be suitable for
these applications.
For the implementation of sensor techniques in
precision crop protection, scale-related issues have to be
taken into consideration (Voss et al. 2010). The spatial,
temporal and spectral demands are tributary to the
measured object and the field of application. For
precision crop protection in the field, airborne sensors,
e.g. mounted to unmanned aerial vehicles, offer large-
scale applications. The use of airborne sensors in
practice, however, is limited by their spatial resolution
and temporal availability of data. Depending on
symptom size and disease severity, patchiness of
primary disease foci and epidemic spread, higher spatial
resolutions may be necessary. Tractor-mounted, non-
imaging sensor systems may provide on-the-move spray
decisions. Based on reflectance measurement and
analysis, application rates may be directly transferred
to the pesticide sprayer.
The technical potential of sensors is expected to
improve in the foreseeable future. However, sensor
use for decision support systems and fungicide
application under field conditions depends also on
our understanding of disease spread, e.g. dispersal
rate of pathogens causing latent infections, zones of
disease risk around primary disease foci, and the
availability of effective fungicides, i.e. ingredients
that effectively control the disease and the spread of
pathogens in order to prevent the disease level from
exceeding the economic threshold level. These
aspects are discussed in more detail by West et al.
(2003).
Eur J Plant Pathol (2012) 133:197–209
Perspectives
An information-driven crop production as a combi-
nation of geospatial and agricultural data management
will encourage the actual utilization of precision
agriculture applications in the future (Reichardt et al.
2009). In terms of precision crop protection different
kinds of optical sensors will play a major role.
Thermography, chlorophyll fluorescence measure-
ments and hyperspectral techniques, alone and in
combinations with sensor fusion approaches can
highlight host-pathogen interactions at an early stage.
This will manage the complexity of an identification
and quantification of different kinds of stressors
(Jones and Schofield 2008). The potential of these
technologies for sensing diseases has not been fully
explored yet. Characteristic signatures of plant dis-
eases based on a multi-sensoral approach may also
contribute to a better understanding of biophysical
and biochemical processes during disease develop-
ment. The link between molecular methods and non-
invasive optical methods could be a new approach,
which has to be tested in future research. West et al.
(2010) demonstrated the use of DNA-based diagnos-
tic methods in air sampling of inoculum for precision
pest management. The interpretation of sensor data,
especially spectral data, nevertheless, is still a limiting
factor for the detection, identification and quantifica-
tion of diseases in crop production. Its implementa-
tion into robust decision support systems by
transdisciplinary cooperation will improve the accep-
tance and realisation of precision crop protection.
Acknowledgement This review is based on activities of
research training group ‘Use of information systems for
precision crop protection’ (RTG 722) at the Faculty of
Agricultural Sciences, Rheinische Friedrich-Wilhelms-
University of Bonn, funded by the German Research Founda-
tion (DFG).
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