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Plant Pathology (2018) 67, 399–410 Doi: 10.1111/ppa.

12741

Automated identification of sugar beet diseases using


smartphones

€hrige,
L. Hallaua, M. Neumannbc, B. Klattc, B. Kleinhenzd, T. Kleind, C. Kuhnd, M. Ro
C. Bauckhageb, K. Kerstingf, A.-K. Mahleina, U. Steinera and E.-C. Oerkea*
a
Institute for Crop Science and Resource Conservation (INRES) – Plant Diseases and Plant Protection, University of Bonn, Bonn; bBonn-
Aachen International Centre for Information Technology, University of Bonn, Bonn, Germany; cDepartment of Computer Science and
Engineering, Washington University in St Louis, St Louis, MO, USA; dCentral Institute for Decision Support Systems in Crop Protection
(ZEPP), Bad Kreuznach; eInformation System for Integrated Plant Production (ISIP), Bad Kreuznach; and fComputer Science Department,
Technical University of Dortmund, Dortmund, Germany

Cercospora leaf spot (CLS) poses a high economic risk to sugar beet production due to its potential to greatly reduce
yield and quality. For successful integrated management of CLS, rapid and accurate identification of the disease is
essential. Diagnosis on the basis of typical visual symptoms is often compromised by the inability to differentiate CLS
symptoms from similar symptoms caused by other foliar pathogens of varying significance, or from abiotic stress. An
automated detection and classification of CLS and other leaf diseases, enabling a reliable basis for decisions in disease
control, would be an alternative to visual as well as molecular and serological methods. This paper presents an algo-
rithm based on a RGB-image database captured with smartphone cameras for the identification of sugar beet leaf dis-
eases. This tool combines image acquisition and segmentation on the smartphone and advanced image data processing
on a server, based on texture features using colour, intensity and gradient values. The diseases are classified using a
support vector machine with radial basis function kernel. The algorithm is suitable for binary-class and multi-class clas-
sification approaches, i.e. the separation between diseased and non-diseased, and the differentiation among leaf diseases
and non-infected tissue. The classification accuracy for the differentiation of CLS, ramularia leaf spot, phoma leaf spot,
beet rust and bacterial blight was 82%, better than that of sugar beet experts classifying diseases from images. How-
ever, the technology has not been tested by practitioners. This tool can be adapted to other crops and their diseases
and may contribute to improved decision-making in integrated disease control.

Keywords: classification algorithm, disease identification, erosion band signature, RGB images, sugar beet

control disease spread (Skaracis et al., 2010). In inte-


Introduction
grated pest management, the use of action threshold
More than 20 fungi and oomycetes and 10 bacterial spe- levels relies on the identification and quantification of
cies have been described as pathogens of sugar beet disease symptoms, preferably in early stages of epi-
(Harveson et al., 2009). At least 10 of these species pro- demics. As several other diseases with considerably lower
duce disease symptoms on sugar beet leaves. Cercospora economic effects may also occur on sugar beet leaves
leaf spot (CLS) caused by Cercospora beticola, a member during the critical period of yield formation, identifica-
of Mycosphaerellaceae, Ascomycota, without a known tion of leaf disease symptoms is crucial for decision mak-
teleomorph, is the most destructive foliar disease of sugar ing in effective CLS control. Induction of pathogen
beet worldwide. There is a high economic risk in terms sporulation in suspect leaf lesions under high relative
of reduced yields and quality of the beet due to the rapid humidity (RH) is associated with the formation of dark
progress of the disease (Weiland & Koch, 2004). pseudostromata considered to be diagnostic for CLS,
Successful CLS management integrates different although it takes at least 12 h of incubation. Despite the
approaches within the cropping system in order to pre- availability of DNA-based and serological methods (De
vent the disease or to reduce severity below the economic Coninck et al., 2012; Dutta et al., 2014), decision mak-
threshold level, i.e. a diversified crop rotation, the use of ing in the field mostly relies on visual inspection and
resistant cultivars, and targeted fungicide applications to identification/classification of leaf symptoms often
encumbered by misidentifications by operators. The
information is then used in decision support systems for
*E-mail: ec-oerke@uni-bonn.de integrated disease management (Wolf & Verreet, 2002;
Racca & Joerg, 2007).
Successful and efficient CLS control requires the rapid
Published online 14 August 2017 and accurate identification of symptoms at low severity

ª 2017 British Society for Plant Pathology 399


400 L. Hallau et al.

in early disease stages in order to control further increase diseases of the crop that may occur simultaneously is
of CLS severity and sugar beet damage by timely fungi- often not included in these approaches.
cide application(s). Reliable identification of plant dis- For a classification of diseases, different approaches
eases is not only important for providing farmers with are available (Behmann et al., 2015). After different pre-
recommendations in terms of integrated pest manage- processing steps, e.g. conversion into another colour
ment, but is also crucial in order to monitor the regional space (Meunkaewjinda et al., 2008; Kai et al., 2011) or
outbreak and spread of diseases. This information can be thresholding (Jian & Wei, 2010), features are extracted
used to predict yield losses and to forecast the temporal from the images. These can be colour, shape or texture
and spatial disease spread, facilitating the coordination features (Anthonys & Wickramarachchi, 2009) that are
of control measures (Racca et al., 2010). then classified by using machine-learning tools like Sup-
Field monitoring of first disease symptoms is the pre- port Vector Machines (SVM) (Youwen et al., 2008) or
requisite for effective disease control, but is also a neural networks (Huang, 2007).
labour-intensive, costly, and somewhat subjective activity None of the aforementioned studies uses a database of
in large-scale fields (Zhou et al., 2014). Diagnosis of the images displaying the natural conditions and variability
disease and identification of the causal agent(s) largely in light, distance or angle, but use a controlled database
depends on expert knowledge and/or long-term experi- (Al Bashish et al., 2010). Barbedo (2014) presented an
ence of the farmer (Nutter et al., 1993). It is crucial to automatic method to detect leaf symptoms of coffee and
identify the causal agent of beet leaf spots as some are of passion fruit using digital images which is simple to
high economic impact and can be controlled by fungi- implement and computationally not complex, but has
cides, whereas others have low impact on sugar yield or the constraint that the background has to be as uniform
may not be controlled because of the lack of effective as possible, nearly black or white.
registered pesticides, e.g. bacterial blight. The diagnosis Furthermore, none of the existing approaches realize a
of sugar beet leaf spots based on machine learning algo- fast and accurate technique of receiving a classification
rithms for processing smartphone images of disease result in real time or enables a partial processing on a
symptoms from the field may substitute for the expert’s smartphone. Unlike the method proposed by Youwen
knowledge, as it is directly available in the field. et al. (2008) that identified just two diseases on cucum-
Automatic detection of diseases may be more efficient ber leaves, the approach proposed in this paper is able to
and accurate than detection or quantification by visual distinguish between five diseases that occur in sugar beet
assessment, which is subjective and often burdened with fields in central Europe (Wolf & Verreet, 2002; B. Klein-
individual errors of estimation. There are several henz, unpublished data):
approaches for greater objectivity in disease assessment
based on digital photography and image analysis or • Cercospora leaf spot caused by the fungus C. beticola
hyperspectral imagery (Bock et al., 2010; Mahlein et al., (Table 1). The pathogen survives in residue from dis-
2012). Barbedo (2016) compared methods to detect, eased plants on the soil (Harveson et al., 2009). Under
quantify and classify plant diseases using image-proces- conditions of leaf wetness and moderate to high temper-
sing techniques on digital images in the visible range of atures, infection starts on the leaves and results in small
the electromagnetic spectrum. For a simple detection of (2–5 mm) round spots with a reddish-purple border and
infested or healthy leaf tissue, approaches such as thresh- a tan to light brown lesion centre (Fig. 1a). There is a
olding or artificial neural networks were applied. Sena definite edge between symptoms and healthy leaf tissue.
et al. (2003) used a thresholding approach to identify The symptoms appear first as single spots that can coa-
maize plants damaged by the fall armyworm based on lesce during disease progress. Under humid conditions
digital images. Abdullah et al. (2007) distinguished the fungus develops black pseudostromata producing
between leaf diseases of rubber trees by using principal conidiophores with long, acicular conidia in the lesion
component analysis combined with neural networks. centre, which may turn greyish (Crous & Braun, 2003).
Leaf diseases may be quantified by visual estimates, • Ramularia leaf spot caused by Ramularia beticola.
e.g. percentage leaf area affected or rating scales (Verei- Typical symptoms are light brown spots of irregular,
jssen et al., 2003; Nutter et al., 2006), and by using vari- more angular shape on the leaves (Harveson et al.,
ous technical approaches, i.e. digital image processing 2009; Fig. 1b). The pathogen infects mostly older
(Camargo & Smith, 2009; Patil & Bodhe, 2011; Atoum leaves and dead tissue and the centre of the leaf spots
et al., 2016), analysis of hyperspectral information may rupture. During prolonged periods of high
(Mahlein et al., 2012) or multispectral images (Cui et al., humidity white conidiophores and conidia can be
2010). Different techniques are applied to the source observed in the centre of the spots (Harveson et al.,
image in different colour spaces to estimate the severity 2009). Ramularia leaf spots are mostly larger and
of the disease. These consist of calculating the ratio brighter than cercospora leaf spots but difficult to dif-
between the number of pixels in damaged regions ferentiate.
divided by the total number of pixels of the leaf after • Phoma leaf spot caused by Phoma betae (teleomorph
discriminating the disease symptoms from healthy leaf Pleospora bjoerlingii). This shows rather large (10–
tissue by thresholding (Skaloudova et al., 2006). Identifi- 20 mm) and light brown, round to oval leaf spots with
cation of the disease and its discrimination from other typical concentric dark rings (Fig. 1c). When several

Plant Pathology (2018) 67, 399–410


Smart disease identification 401

spots are present, they can grow together and form

(to medium)

(to medium)
larger blotches and dead tissue can collapse.
Economic
• Beet rust caused by Uromyces betae. Small round
impact
High

Low

Low

Low

Low
pustules bear the reddish-brownish urediniospores


(Fig. 1d).
Fungicides

Fungicides
• Bacterial blight of sugar beet caused by Pseudomonas

available
Control

syringae pv. aptata. This is the only bacterial disease

Not
occurring regularly in Germany (Riekmann & Steck,


1995). Mechanical damage from hail, in particular,
Overall
20–30

16–20

15–32

15–22

10–25
promotes disease incidence, as the bacteria enter
requirement (°C)


plant tissue through wounds or stomata. Bacterial
Temperature

leaf spots are typically dark brown to black, irregular


Infection

in size and shape and individual spots often show a


12–37

5–25


light interior (Fig. 1e). Spots of P. syringae pv. aptata
and C. beticola often look very similar and are thus
difficult to distinguish.
Hyaline, through
Conidiophores

This paper presents a novel approach to automati-


stomata

cally classify five diseases of sugar beet based on RGB


(red-green-blue) images recorded with a smartphone.
Dark

The images are recorded under field conditions and the


algorithm used goes beyond detection or quantification


Sporulation (100% RH)

multicellular, needle-

of disease symptoms, and is able to classify the diseases


urediniospores in
uredia rupturing

using simple texture features and second-order statistics.


Hyaline, slender,

Hyaline, whitish,

conidia in dark
1-celled hyaline

Reddish brown

Furthermore, this approach is automated and fast.


epidermis
pycnidia
2-celled
Table 1 Characteristics of leaf diseases of sugar beet frequently occurring in Germany and neighbouring countries

Spores

Materials and methods


like

Image database
concentric dark rings
Light brown centre,

Dark brown, lighter

For the development of the recognition algorithm, a compre-


Reddish to brown,
Tan to light brown
centre, brown to

hensive image database covering the variability of several dis-


purple border

brown border
Light brown,

ease symptoms was established. Images of CLS and other sugar


yellow halo

beet leaf diseases were recorded in experiments under con-


Variable
centre
Colour

trolled and field conditions using >40 cultivars of sugar beet,


two fertilizer levels (0 and 180 kg N ha1), various growth
stages of sugar beet (and leaf diseases), different light condi-
Diameter

tions and various distances between object and camera lens (=


Irregular
10–20

spatial resolution). Images were taken in the growth periods


(mm)
2–5

4–7

1–3

2012 and 2013 with different smartphone camera types,


including a Samsung GT-I9300 (Samsung Electronics GmbH),
a Sony Ericsson LT18i (Sony Mobile Communications AB) and
Round to angular

a Motorola DEFY + (Motorola Inc.) differing in the spatial


Round, slightly
Round to oval

resolution of the cameras (8, 8 and 5 megapixels, respectively).


Symptoms

Irregular

Under field conditions (site Kerpen, Germany, in 2012 and


Variable
raised
Round
Shape

2013), disease symptoms from untreated plots of 48 different


cultivars were recorded. Under controlled conditions, 13 culti-
vars differing in susceptibility to the leaf diseases were used.
The resulting database comprised images displaying a great
syringae pv. aptata
Cercospora beticola

Ramularia beticola

variety of sugar beet leaf symptoms and of conditions of image


Uromyces betae

recording. The images were stored in the RGB colour space in


Phoma betaea

Pseudomonas

Teleomorph Pleospora bjoerlingii.

JPG format. The database included symptom images of five


Pathogen

leaf diseases of sugar beet as well as images of healthy leaves,


and comprised non-diseased leaves (450 images), CLS (720),
ramularia leaf spot (200), phoma leaf spot (30), beet rust (220)

and bacterial blight (250). To ensure the ground truth informa-


tion of each leaf spot used to train the algorithm for further
Abiotic disorders
Phoma leaf spot
Cercospora leaf

Bacterial blight

processing, spots were, if needed, identified/confirmed micro-


Ramularia leaf

scopically, and then annotated manually. A simple annotation


Beet rust

program was designed using the software MATLAB (MathWorks


Disease

Inc.). This software was also used for further processing of the
spot

spot

image-processing algorithm.
a

Plant Pathology (2018) 67, 399–410


402 L. Hallau et al.

(a) (b) (c) (d) (e)

Cercospora leaf spot Ramularia leaf spot Phoma leaf spot Beet rust Bacterial blight

Figure 1 Smartphone images of sugar beet leaves showing typical leaf spots caused by five different pathogens. [Colour figure can be viewed at
wileyonlinelibrary.com]

• Computation of a region image R from image B to subsume


Identification of the pathogens median filtering of image B, connected component analysis,
To identify the different pathogens, infected leaves collected hole filling, filtering of regions adjacent to the image borders,
from the field and from controlled conditions were incubated as well as filtering of regions where the width/height ratio is
under 100% RH for 48 h. After this time period, the causal not in the interval [0.7: 2]. The latter is motivated from bio-
agent of each disease symptom was identified under a logical expertise because leaf spots tend to be compact and
stereomicroscope (M7 16F; Leica) based on the structure of regions that are too elongated can be discarded from further
conidia and conidiophores. Lesions without fungal structures analysis (Fig. 2e).
were assumed to be of bacterial origin. For positive identifica- • Suppression of all pixels in image D that are background pix-
tion of P. syringae pv. aptata, surface-sterilized leaf spots were els in image R; the information in the new image G forms the
incubated on malt extract agar (Merck). After 3–4 days at basis for the subsequent analysis.
22 °C, the typical bacteria colonies could be observed. The
A detected region was defined as a connected component in
software DISKUS (Carl H. Hilgers) was used to take and orga-
image G and the following steps of the algorithm were per-
nize microscopic pictures.
formed on each detected region separately.

Development of image-processing algorithm Feature computation


The extracted regions from the region detection step were the
The developed algorithm for classifying beet disease symptoms basis for feature computation and classification. As a first step,
from RGB images basically consisted of three steps: (i) region each region was scaled such that its larger image dimension
detection, (ii) feature extraction, and (iii) class prediction. The measured 75 pixels. The approach of feature computation uses
extraction of regions was the only step in this procedure which texture features instead of established shape descriptors and
was applied to the whole input image, whereas computation of shape recognition methods, such as form factors (Gonzales &
features and classification were performed on the extracted Woods, 2008), bounding box signatures (Bauckhage, 2006), or
regions only. entropies of curves (Ebrahim et al., 2007). This is due to the
lack of discriminative power for the task of leaf spot classifica-
Region detection tion as the leaf spots are typically difficult to distinguish by their
Region detection is an important step in the image processing forms and sizes. The image database considers different time
procedure because the subsequent steps of feature extraction can points and thus sizes and forms of spots and does not assume a
only be applied on the detected regions and thus are dependent particular stage of infection. Therefore, features based on col-
on the accuracy of detection. To obtain useful intermediate rep- our, intensity and gradients were used in order to classify the
resentations for later steps, a strategy of several pre-processing image regions by considering the colour values and intensity
steps proved to be successful. The following steps were applied changes within the regions. From the original RGB values of
to the images from the database: each region the following values were computed: (i) red-channel
(R), (ii) green-channel (G), (iii) blue-channel (B), (iv) intensities
• Down-scaling of the input image I (Fig. 2a) by 25% to increase (INT), (v) local binary patterns (LBPs) of intensities (INTLBP),
sharpness and to facilitate further computation. The size of the (vi) gradient magnitudes (Gmag), (vii) gradient directions (Gdir),
resulting image D was 484 9 648 pixels 9 3 colours (0.94 MB) or and (viii) LBPs of gradient magnitudes (Gmag LBP). LBP descrip-
612 9 816 9 3 (1.5 MB), depending on the type of smartphone tors (Ojala et al., 2002) provide an efficient way to characterize
camera (Fig. 2b). local textures and numerous references in recent literature report
• Application of a maximum RGB filter to image D in order to high- on their potential to enable a highly accurate classification of
light reddish/brownish image regions that may point to leaf spots the components of RGB images (Maturana et al., 2009).
caused by fungi or bacteria (Fig. 2c). Based on the colour and gradient information of the extracted
• Computation of a binary image B from the RGB-filtered regions, simple and co-occurrence-based statistical texture fea-
image such that reddish pixels become foreground pixels and tures were computed. First-order statistics such as mean, vari-
greenish/blueish pixels become background pixels (Fig. 2d). ance or entropy lead to simple characteristics of image texture.

Plant Pathology (2018) 67, 399–410


Smart disease identification 403

(a) (b) (c) (d) (e)

Smartphone Max RGB values Colour-filtered Binary region Extracted region


image image image image

Figure 2 Smartphone camera image of a sugar beet leaf infested by Phoma betae (a) and different pre-processing steps for extracting regions of
interest. [Colour figure can be viewed at wileyonlinelibrary.com]

Second-order statistics computed from the spatial co-occurrence features, whereas more than four unnecessarily increases the fea-
of pixel values can describe the texture of an image by analysing ture dimensionality. Further discussion and detailed formulas
relationships among pairs of pixels. This characteristic makes were provided by Neumann et al. (2014).
second-order statistics a powerful tool for texture description
and seven values were applied: (i) correlation, (ii) entropy, (iii)
inverse difference moment, (iv) variance, (v) sum entropy, (vi)
Classification of symptoms
difference entropy, and (vii) sum variance. Predicting the disease of each region based on the set of com-
puted features, a one-versus-one multi-class support vector
In addition to the first- and second-order statistics computed
on the different colour-, intensity-, and gradient-channels, ero- machine (SVM) using the radial basis function (RBF) kernel
sion band features were considered for the computation of fea-
tures. The use of erosion band features (Vazquez et al., 2013) jjx  x0 jj2
should take into account the more or less round shape of the kðx; x0 Þ ¼ expð Þ ¼ expðcjjx  x0 jj2 Þ
2r2
leaf spots and should result in additional fine-grained texture
features. Erosion bands are applied to the extracted region, was trained. kx  x0 k2 is the squared Euclidean distance
whereas the erosion width can be deduced from a given number between the feature vectors of the samples x and x0 . r is a free
of iterations and the region dimensions. Four erosion steps were parameter defining the width of the Gaussian kernel. For all
applied to each extracted region to subsequently compute the experiments the SVM-cost parameter c and the kernel parameter
texture descriptors on each erosion band (Fig. 3). The use of c were learned via 10-fold cross-validation on the respective
fewer than four erosion steps produces less discriminant training splits.

(a) Erosion bands

(b) Eroded RGB regions

Figure 3 Application of erosion bands (a) of a cercospora leaf spot for the extraction of relevant RGB information (b) from band-like patterns.
[Colour figure can be viewed at wileyonlinelibrary.com]

Plant Pathology (2018) 67, 399–410


404 L. Hallau et al.

The considered parameter ranges are c = e {23, 22, . . . , 26} (Kohavi & Provost, 1998), was used to evaluate the approaches
and ce {0.01, 0.05, . . . 5.0, 10.0}. The classifier was trained on described above.
six classes, from which five were leaf diseases of sugar beet: cer- Sensitivity or true positive rate (TPR) was calculated as:
cospora leaf spot (CERCLS), ramularia leaf spot (RAMULS),
beet rust (BEETRU), phoma leaf spot (PHOMLS) and bacterial TPR ¼ TP=ðTP þ FNÞ;
blight (BACTBL). The sixth class was non-diseased (N-DIS) leaf
tissue and was introduced to handle regions extracted by the whereas specificity or true negative rate (TNR) was calculated
region detection step not belonging to one of the five disease as:
classes. This class may include healthy leaf parts, such as reflec-
tions or leaf veins, soil particles on the leaf, the ground, or holes TNR ¼ TN=ðFP þ TNÞ
in the leaf. These regions occur as the applied region detector
works based on a max RGB filter that selects the reddish parts Accuracy (ACC), i.e. the proportion of the total number of
of the image. correct predictions, was calculated as:
In addition to the classification of diseases considering the six
classes described, there was also a binary task analysing the dis- ACC ¼ ðTN þ TPÞ=ðFN þ FP þ TN þ TPÞ
ease detection rate. In this approach only the classes ‘diseased’
(DIS) and ‘non-diseased’ (N-DIS) were considered, where DIS with FN = false negative, FP = false positive, TP = true positive,
subsumed all regions that were of any of the five diseases. This and TN = true negative.
approach describes a simple disease detection rate without any
classification (= differentiation among diseases). Therefore a
SVM with the same kernel settings as described above was used. Results
The extensive feature study for determining a small, but
Feature study meaningful feature combination for robust leaf spot clas-
sification from RGB images was conducted on a set of
A first feature study (STUDY) was implemented to figure out training data. This feature combination was then evalu-
which combination of features was the most powerful for ated on a comprehensive dataset (FULL) of almost 3000
disease classification. A small dataset that included equal
regions.
amounts of regions for each disease was selected from the
entire image database. It consisted of 296 regions extracted
from 495 images considering regions of only one single leaf Feature selection process
spot (Table 2).
The features described above were applied on this selected The average accuracies for all feature/value combinations
dataset and the most successful combination of features was implemented for the feature study are shown in Table 3,
chosen. Therefore, the performance of each feature combination including: (i) computations on total regions or on erosion
was evaluated by using the described classification method of bands; (ii) intensity-, colour- and gradient-based values;
SVM on 20 randomly generated but fixed data splits. and (iii) first-order and second-order statistics. The can-
didates for the final feature collection included the best
Survey on the accuracy of disease identification by performing pairs in each group (values in bold in
sugar beet experts Table 3).
The local binary pattern (LBP) images of intensities
In spring (March/April) 2015, 27 experts from the fields of (INT) and gradient magnitudes (Gmag) improved the per-
sugar beet production and crop protection services were asked formance of ‘mean’ and ‘entropy’. Comparing the perfor-
to identify leaf diseases of sugar beet from images used for
mances of first- and second-order statistics, the latter
training the algorithm. In an online survey they had access to
30 images with various leaf spots: 8 for CLS, 2 for beet rust,
gave higher accuracies. As distances (d) >1 decreased the
7 for bacterial blight, 11 for ramularia leaf spot and 2 for accuracy, the relation between neighbouring pixel pairs
phoma leaf spot. In the course of the survey the class ‘Not includes important information for the classification of
sure’ was included in order to express the uncertainty of the leaf spots.
experts. In order to build a small and powerful feature collec-
tion including a broad range of diverse features, the final
feature collection was derived from forward selection fol-
Statistical evaluation
lowed by backward elimination on the values indicated
A confusion matrix containing information about actual and in bold. This resulted in the erosion feature ensemble
predicted classifications determined using a classification system (EFE) representing the combination of erosion band

Table 2 Number of regions per class in the


N-DIS CERCLS BEETRU BACTBL RAMULS PHOMLS Total
datasets STUDY and FULL
STUDY 55 57 47 44 57 36 269
FULL 1105 1006 72 494 225 55 2957

N-DIS, non-diseased; CERCLS, cercospora leaf spot; BEETRU, beet rust; BACTBL, bacterial
blight; RAMULS, ramularia leaf spot; PHOMLS, phoma leaf spot.

Plant Pathology (2018) 67, 399–410


Smart disease identification 405

Table 3 Average accuracies obtained from 20-fold cross validation on the STUDY dataset

Dim. Int. (1) Int. LBP (1) R (1) G (1) B (1) RG (2) RB (2) GB (2) RGB (3) Gmag (1) Gdir (1) Gmag LBP (1)

Total region
Mean 1 35.1 42.4 32.7 41.5 42.9 42.2 42.9 43.1 47.0 21.6 32.4 35.5
Variance 1 23.3 20.0 21.4 30.3 23.6 36.8 35.7 34.4 43.5 30.5 25.7 19.6
Mean & variance 2 37.5 42.0 30.6 37.1 47.9 44.1 49.6 46.9 54.3 41.2 33.4 36.1
Entropy 1 35.6 43.3 33.3 34.7 30.3 35.3 36.1 45.3 44.5 34.8 49.0 44.2
Texture (d = 1) 7 57.4 52.8 59.3 56.7 58.8 65.9 65.5 64.4 68.2 51.9 48.7 48.7
Texture (d = 3) 7 50.0 48.4 51.2 50.3 48.5 62.8 57.0 54.5 62.4 48.2 49.3 45.8
Texture (d = 5) 7 49.5 50.8 48.9 43.5 46.9 57.7 54.6 52.6 57.0 49.3 46.2 41.2
Erosion bands
Mean 4 54.5 50.5 49.2 54.6 52.6 54.3 53.2 56.0 54.6 42.8 30.7 43.9
Variance 4 45.1 29.0 42.5 45.1 45.5 52.6 50.7 44.5 52.3 36.7 38.2 32.8
Mean & variance 8 58.7 51.0 56.6 60.1 55.4 60.8 59.0 60.4 61.7 48.3 37.1 42.8
Entropy 4 43.2 54.0 44.5 42.8 47.2 47.3 50.0 50.3 55.3 47.2 43.6 52.9
Texture (d = 1) 28 67.7 55.4 69.0 65.8 64.8 71.8 68.8 71.3 71.9 48.9 51.4 53.7
Texture (d = 3) 28 62.4 54.4 67.0 67.1 60.7 69.1 66.8 63.8 67.7 47.2 51.4 44.2
Texture (d = 5) 28 63.8 57.8 66.2 65.5 62.5 69.1 68.8 64.2 70.9 47.2 48.0 46.6

Membership in the candidate feature set for the erosion feature ensemble (EFE) described in Results is indicated in bold.

‘texture’ descriptor (d = 1) on the three colour channels leaf diseases, CERCLS, RAMULS, BEETRU, PHOMLS
(RGB) and gradient magnitude LBPs (Gmag LBP). EFE and BACTBL (i.e. multi-class task).
had 112 dimensions and gave 75% classification accu- The application of the described feature combination
racy on dataset STUDY. EFE in the binary classification task of disease detection
produced an average accuracy of 93.1%, compared to an
accuracy of 94.6% for the STUDY dataset (cf. Table 4).
Performance of EFE on FULL dataset
A random class assignment in this binary task would
The EFE feature combination was applied on a dataset lead to an accuracy of 50.0%, significantly lower than
of 2957 regions extracted from the same 495 images as accuracy yielded from the EFE feature set.
the STUDY dataset. This bigger dataset did not consider In the multi-class task of disease classification, the EFE
any balance between the disease classes, and also feature combination resulted in an average accuracy of
included coalesced leaf spots (Fig. 4). 83.7% for the FULL dataset compared to 75.2% for the
Two objectives were addressed: (i) disease detection, STUDY dataset. Random assignment for the six classes
whether a leaf spot is due to a plant pathogen or not leads to an accuracy of 16.7%.
(i.e. binary task); and (ii) disease classification in order Comparing the accuracies of each class for both data-
to distinguish between non-diseased tissue and the five sets, the classification accuracy for almost all classes

(a) (b) (c)

Bacterial blight Cercospora leaf spot Ramularia leaf spot

Figure 4 Examples of regions of interest with coalesced spots of three different sugar beet leaf diseases. [Colour figure can be viewed at
wileyonlinelibrary.com]

Plant Pathology (2018) 67, 399–410


406 L. Hallau et al.

Table 4 Accuracies of the erosion feature ensemble (EFE) and the two economic significance of the disease and whether it can
baseline methods, most frequent class (MFC) and random (RAND), for be controlled directly by chemical means or not.
the detection and classification of sugar beet leaf diseases on datasets Although progress has been made in the classification of
STUDY and FULL
plant diseases from images, the majority of methods are
– if at all – only capable of discriminating among a small
Disease detection Disease classification
number of diseases (reviewed in Barbedo, 2016). This
Dataset EFE MFC RAND EFE MFC RAND paper presents a novel approach for the detection and
STUDY 94.6 ( 5.6)a
81.5 50.0 75.2 ( 8.6) 19.3 16.7 classification of leaf spot diseases of sugar beet based on
FULL 93.1 ( 2.3) 62.5 50.0 83.7 ( 3.2) 37.5 16.7 the computation of statistical texture features considering
multiple erosion bands of an extracted image region. An
a
Mean ( SD). Bold font highlights the superiority of the accuracy of extensive feature study allowed the identification of the
EFE compared to the accuracies expected for MFC and RAND.
best performing combination of features. The approach
assigns the process to a smartphone in the field and an
increased with the number of underlying data. All classes in-house server for image recording, region detection and
except PHOMLS had a classification accuracy >68%, communication with the server, and computationally
and the classes non-diseased and BEETRU had a classifi- intensive feature extraction and classification algorithms,
cation accuracy >90%. The confusion matrix in Table 5 respectively (Fig. 5).
summarizes the positive and negative classification results By using smartphones for image recording in the field,
for the FULL dataset and highlights the higher rate of the variability of disease symptoms due to the interaction
mismatches for PHOMLS (and RAMULS). between the host, pathogen and environment (Zhou
et al., 2014; Barbedo, 2016) is complicated by the factor
image recording conditions, e.g. illumination. However
Performance of sugar beet experts in classification of
the quality and spatial resolution of modern smartphone
disease images
cameras were not an issue in disease identification. The
The experts in sugar beet production and crop protection approach of detecting the regions on the smartphone
advisers evaluated 30 images of sugar beet leaf segments itself was due to the demand for the algorithm to be sim-
with one tagged disease symptom each. The overall accu- ple and efficient enough to be able to work on a smart-
racy of the 27 experts was 46.4% (Table 6). Prevalence phone. None of the steps in the processing cascade for
of the class ‘Not sure’ demonstrates the problem of dis- the region detection makes use of floating point opera-
ease diagnosis from images. Leaf rust was diagnosed tions, each intermediate step can be computed using only
with high sensitivity and 100% specificity, whereas bac- integer arithmetic. This makes it possible to implement
terial blight and the mix-up of CLS and ramularia leaf the steps on earlier generation smartphones, which do
spot were the greatest problems for the experts. not have capacity for floating point units.
The extraction of regions of interest (ROIs) on the
smartphone reduces the data size to be sent to the ana-
Discussion
lysing platform. On the server the extraction of features
Several crop diseases may occur simultaneously in a field, and disease classification is applied to each of these
on the same plant, even on the same leaf. The diagnosis ROIs, not to a complete image or multiple regions. The
of the disease(s) is crucial in crop protection – and has same method gave success in the classification of leaf dis-
priority to disease quantification – as the nature of the eases of cucumber, where the best classification was
disease (and its causal agent) determines the potential reached by taking each spot as a sample instead of each

Table 5 Confusion matrix for the analysis of Erosion Feature Ensemble for the classification of five sugar beet leaf diseases and non-diseased tissue
from the FULL dataset

N-DISa CERCLS BEETRU BACTBL RAMULS PHOMLS Total TNRb

N-DIS 1009 26 2 58 15 6 1116 0.904


CERCLS 39 891 0 94 28 14 1066 0.836
BEETRU 2 0 65 1 0 0 68 0.956
BACTBL 44 64 5 335 17 3 468 0.716
RAMULS 9 24 0 6 163 16 218 0.748
PHOMLS 2 1 0 0 2 16 21 0.762
Total 1105 1006 72 494 225 55 2957 –
TPRc 0.913 0.886 0.903 0.678 0.724 0.291 – 0.838

a
N-DIS, non-diseased; CERCLS, cercospora leaf spot; BEETRU, beet rust; BACTBL, bacterial blight; RAMULS, ramularia leaf spot; PHOMLS, phoma
leaf spot.
b
True negative rate (= specificity).
c
True positive rate (= sensitivity).

Plant Pathology (2018) 67, 399–410


Smart disease identification 407

Table 6 Confusion matrix for the analysis of


CERCLSa BEETRU BACTBL RAMULS PHOMLS Total TNRb
the classification of five sugar beet leaf
diseases by 27 experts in sugar beet CERCLS 112 2 69 47 1 231 0.485
production. Thirty images with leaf diseases BEETRU 0 44 0 0 0 44 1.000
were classified in an online survey, July BACTBL 26 1 62 17 10 116 0.534
2015 RAMULS 35 1 16 131 15 198 0.662
PHOMLS 28 1 8 86 27 150 0.180
Not sure 15 5 34 16 1 71 –
Total 216 54 189 297 54 810 –
TPRc 0.519 0.815 0.328 0.441 0.500 – 0.464

a
CERCLS, cercospora leaf spot; BEETRU, beet rust; BACTBL, bacterial blight; RAMULS,
ramularia leaf spot; PHOMLS, phoma leaf spot.
b
True negative rate (= specificity).
c
True positive rate (= sensitivity).

Smartphone
in the field
Image acquisition

Transmission
of ROIs Feature
extraction
Region detection

Classifica-
Forwarding tion (SVM)
of results
Bacterial blight
Beet rust
Cercospora leaf spot
Phoma leaf spot
Ramularia leaf spot In-house server

Figure 5 Schematic representation of data processing for the automated identification of sugar beet leaf diseases based on smartphone images.
Image recording with smartphone camera in the field, image segmentation and reduction of data, transfer of regions of interest (ROIs) to server,
analysis and classification of data on the server, forwarding of classification result to the smartphone in the field. [Colour figure can be viewed at
wileyonlinelibrary.com]

entire leaf (Jian & Wei, 2010). The automated identifica- conditions of image collection. By contrast the method
tion of disease symptoms from smartphone images is described here is quicker, has minimal computational
rapid – the classification result on the nature of the leaf requirements and is based on images collected under less
spot is available within minutes – and needs no extra well-defined conditions.
equipment for the farmer in the field. It is non-destruc- The approach of an automatic method to detect leaf
tive and requires neither the handling of biochemicals or diseases of coffee and passion fruit using digital images
specialized test kits in the field, nor sampling and storing (Barbedo, 2014) is afflicted with the necessity of a uni-
of biological material for further analysis in the labora- form background. The approach presented here does not
tory. require any special backgrounds or other limitations. A
Bauer et al. (2011) used multispectral images merged format filling view of the leaf and its spots is advanta-
with RGB images to compare different automatic meth- geous, but not compulsory. Images of disease symptoms
ods to detect sugar beet leaf diseases. Depending on the on the leaf level avoid many background problems; how-
classification method, they reached classification rates of ever, segmentation of regions of interest has to be done
up to 91% for CLS detection. This approach used and this approach does not allow disease quantification.
advanced techniques for image acquisition and the merg- Zhou et al. (2015) proposed a three feature combi-
ing of images, but was computationally demanding, nation L*, a*, entropy 9 density, for CLS classifica-
time-consuming and was conducted under controlled tion and also showed promising results in the field. In

Plant Pathology (2018) 67, 399–410


408 L. Hallau et al.

combination with single leaf tracking based on robust texture features in the model system sugar beet leaves
template matching by orientation code matching, the has prompted investigations to apply similar techniques
algorithm was suitable to follow disease development, for disease classification in other crops, such as wheat or
but without checking the identity of the leaf spots. Previ- maize. The methodology showed promising primary
ously these authors used a single-feature two-dimensional results, at least for roundish disease symptoms, e.g. early
xy-colour histogram as input for pixel-wise SVM classifi- septoria leaf blotch.
cation of CLS (Zhou et al., 2014). The additional use of The diagnosis of crop diseases/plant pathogens has to
texture features obviously increased the robustness of the be complemented by disease quantification in order to
detection algorithm. deduce a control decision. Manual systems for CLS rat-
The results reported here prove the high adequacy of ing in the field may be also subjective, laborious and rel-
the selected feature combination EFE not only for the atively insensitive to subtle variation of the leaf spot
simpler task of disease detection, but also for the identifi- appearance (Afridi et al., 2014). These authors developed
cation of leaf spots caused by various fungal and bacte- a computer vision system, CLS Rater, to automatically
rial pathogens. Although convincing for CLS, the main and accurately rate CLS of whole-plant images in the
purpose of this study, the results lead to an assumption field according to the 0–10 USDA scale of Ruppel &
that higher accuracies for different classes, i.e. PHOMLS Gaskill (1971). Experimental results showed CLS Rater
or RAMULS, can be achieved by considering more to be highly consistent with a rating error of 0.65 com-
regions/images of these diseases. However, these two dis- pared to 1.31 by human experts (Atoum et al., 2016).
eases have been rare in sugar beet fields in Germany in The role of smartphone images in decision support
recent times, although they have been reported to be an systems may be not limited to the identification of dis-
economic problem in other periods of time (Maerlaender eases in sugar beet or other crops. Additional data on
et al., 2003) and other regions (Thach et al., 2013). The the phenological stage of the crop and positioning data
shortage of sufficient training data for PHOMLS and the may improve disease monitoring on various spatial
misclassification of phoma leaf spots as cercospora leaf scales. The use of smartphone applications facilitates
spots or ramularia leaf spots are probably the reasons and improves the communication between farmer and
for the low accuracy for PHOMLS in the evaluation extension services and may contribute to an online
step. The portion of PHOMLS in the total dataset was approach of integrated disease management by provid-
considerably lower than in the balanced STUDY dataset. ing online data on disease incidence and weather-based
The problem of low representations of disease symptoms disease forecasting as major input data of decision sup-
may be overcome by databases such as the collection of port systems.
disease images for crops developed by Hughes & Salathe
(2015). Acknowledgements
The feature design regarding the erosion bands goes
beyond the use of descriptors simply computed on whole The project was supported by funds of the German Fed-
extracted regions as previously used for plant disease eral Ministry of Food and Agriculture (BMEL) based on
classification. Erosion band signatures are a codification a decision of the Parliament of the Federal Republic of
of the spatial coherence of features extracted from a Germany via the Federal Office for Agriculture and Food
region that is often lost in feature extraction methods (BLE) under the innovation support programme (project
(Vazquez et al., 2013). The problem of coalescent leaf ID 2815411310).
spots that frequently occur in later stages of the growth
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