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Assessing mango anthracnose using a new three‐dimensional image‐analysis

technique to quantify lesions on fruit

Article in Plant Pathology · December 2005

DOI: 10.1111/j.1365-3059.2005.01321.x

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Plant Pathology (2006) 55, 250–257 Doi: 10.1111/j.1365-3059.2005.01321.x

Assessing mango anthracnose using a new

Blackwell Publishing Ltd

three-dimensional image-analysis technique to

quantify lesions on fruit

G. Corkidia*, K. A. Balderas-Ruízb, B. Taboadaa, L. Serrano-Carreónb and E. Galindob

a
Image Analysis Laboratory, Centro de Ciencias Aplicadas y Desarrollo Tecnológico, UNAM; and bDepartment of Cellular Engineering
& Biocatalysis, Instituto de Biotecnología, UNAM, Avenida Universidad 2001, Colonia Chamilpa, 62250, Cuernavaca, Morelos, México

An accurate image-analysis method was developed to assess quantitatively the spot-like lesions on fruits resulting from
pathogen attack. The technique was applied to evaluation of the development and severity of anthracnose of mango fruit,
caused by the fungus Colletotrichum gloeosporioides. In this method, a stepper motor rotates the mango fruit along its
longitudinal axis while acquiring a sequence of 360 images of its total surface (one image for each degree). This set of
images is used to create a pseudocylindrical ‘equal-area’ projection of the fruit in a two-dimensional map containing
complete morphometrical and photometrical information of its surface. The lesion area can easily be evaluated from
this map with image-analysis procedures. Quantitative data (percentage of area affected) can be used to establish an
assessment scale for the disease based on lesion spots measured, as well as for detailed laboratory studies of mango
anthracnose development. The average error of the method is −0·1%, standard deviation 0·44 (r 2 = 0·99), and it may
be adapted for use with most commercial image analysers and for other diseases with spot-like symptoms.

Keywords: anthracnose, fruit-disease development, image analysis, pseudocylindrical projection, spot lesions,
three-dimensional area measurement

as rounded, brown to black lesions which can converge

Introduction
Mango (Mangifera indica) production is very important
in Asia and in Latin American countries including Mexico
and Brazil. International trade in mango is dominated by
certain varieties such as Keitt and Tommy Atkin (FAO,
2003). Anthracnose is the major pre- and postharvest dis-
ease of mango, caused by Colletotrichum gloeosporioides
(teleomorph: Glomerella cingulata) (Arauz, 2000), and
can result in serious decay of fruit during marketing and
after sale.
Incidence of infection by this pathogen is favoured by
temperatures ranging from 20 to 30°C and a relative
humidity >95%, and it has been observed on panicles,
leaves and fruits (Dodd et al., 1991). Panicle anthracnose,
or blossom blight, can affect the inflorescence stalk and
individual flowers in the preharvest phase. Postharvest
anthracnose occurs when the young fruit has been
infected in the field, and remains in a quiescent stage until
fruit ripening begins (Prusky, 1996). The symptoms appear
*E-mail: corkidi@ibt.unam.mx
Accepted 21 July 2005
and cover extensive areas of the mango fruit surface.
These lesions are generally evident during storage, when
the fruit is in the maturation phase, and are usually
restricted to the peel. However, in severe cases the fungus
can invade the pulp. In advanced stages of the disease, the
fungus produces acervuli and abundant orange to salmon-
pink masses of conidia on lesions (Arauz, 2000).
Traditionally, in order to evaluate the severity of the dis-
ease (Smoot & Segall, 1963; Brodrick, 1978; Koomen &
Jeffries, 1993), visual ‘hedonic’ scales (subjective testing
carried out by trained evaluators) are used (http://
food.oregonstate.edu/sensory/dena.html). This kind of
evaluation is qualitative and subjective, as it depends on
the experience of the evaluators. In particular, a widely
used technique (Brodrick, 1978) involves assessment
scales (1–5) based on the evaluation of percentages of the
area affected in the fruit: 1, <1%; 2, 1–5%; 3, 6–9%; 4,
10–49%; 5, 50–100% of the area affected by anthracnose
lesions. However, such ‘percentages’ are not determined
quantitatively, but rather are based on the visual appreci-
ation of an expert. This is a serious drawback as it is very
difficult to standardize methods among different evaluators
and laboratories. Image analysis can contribute to solving
this problem, and recently Diéguez-Uribeondo et al. (2003)

250 © 2005 BSPP

 Image analysis of lesions on mango fruit
Figure 1 Image-analysis apparatus: (a) fruit;
(b) plastic fruit support; (c) stepper motor;
(d) stepper motor control module; (e) CCD RGB
TV camera; (f) 300-W incandescent lamp;
(g) computer screen; (h) anthracnose traces;
(i) white background screen illuminated with
60-W incandescent lamp (not shown);
(j) joystick to rotate fruit manually for vertical
axis alignment and setting the initial position
of fruit.
used the technique to help understand the penetration
and infection process of Colletotrichum acutatum and
to determine the conditions favouring anthracnose in
almonds. Although a great variety of image-analysis
software is commercially available (Malamas et al., 2003),
including specific applications in phytopathology (Lamari,
2005), no quantitative 3D imaging techniques have been
reported in the literature for the characterization and
assessment of fruit diseases. The aim of this work was
to develop and to apply an accurate method, based on
three-dimensional image-analysis techniques, to evalu-
ate quantitatively the development of spot-like lesions on
the surface of fruits. The potential of the technique was
tested using mango fruit anthracnose.
Materials and methods
Inoculation of fruit and development of anthracnose
Colletotrichum gloeosporioides was grown on potato
dextrose agar (PDA, Difco) and incubated at 29°C.
Conidia of 7-day-old cultures, washed from the surface
of plates with NaCl and Tween 80 solution (0·85%
and 0·05% wt/vol, respectively), were used as inoculum.
Prior to C. gloeosporioides inoculation, all fruits were
surface sterilized with a 1% NaOCl solution for 10 min,
then washed with distilled water and allowed to dry.
The effect of the level of inoculation of the pathogen
was assessed. Suspensions (5 mL) of C. gloeosporioides
containing either 105, 106 or 107 conidia mL−1 were applied
to 10 mango fruits (variety Manila) with an aerosol spray
bottle, each time in triplicate. A randomized block experi-
ment was carried out in order to evaluate the effects of the
treatment (inoculum concentration) and of time (block).
An anova was performed to evaluate significant differ-
ences among treatments. After inoculation, the mangoes
© 2005 BSPP Plant Pathology (2006) 55, 250–257
251
were allowed to dry and were stored in conditions
favourable for disease development (25°C, 95% RH) in
a storage chamber (Environ-Cab 680, Laboratory-Line
Instruments, USA). Anthracnose severity was evalu-
ated daily, for 10 days’ incubation, as the percentage of
anthracnose-affected area per fruit. The distribution of
the equivalent diameter of spots (diameter of an equiva-
lent perfect circle containing the measured object’s area)
was also evaluated daily.
Image analysis
A mango fruit was placed on a nylon support with a central
cavity where the peduncle of the fruit was positioned. This
support (Fig. 1) was mounted into the axis of a DC
stepper motor attached to a FOCMCMST 73005056
Step-Foc Motor control module (Ludl Electronic Products,
Hawthorne, NY, USA). This module was controlled with
a LEP MAC5000 PS-System 73005020 (Ludl Electronic
Products) and connected to a Pentium 4 computer via
an RS232-USB 73005042 module (Ludl Electronic Prod-
ucts). The DC stepper motor can also be activated manu-
ally with the digital potentiometer for focus control of an
XY joystick (Ludl Electronic Products). This hardware is
commonly used in the motorized stages of optical micro-
scopes, and the z axis (focusing device) was used only for
moving the fruit. The image-acquisition hardware was
composed of a COHU high-performance RGB colour
CCD camera 8295-2000/0000 (Cohu Electronics Division,
USA) and a frame-grabber Flash Point 128 (Integral Tech-
nologies, USA). The instructions to drive the stepper
motor were implemented from the Scope-Pro module
(Media Cybernetics, USA) and executed within the
image-pro plus 4·45 software (Media Cybernetics),
under windows xp (Microsoft, USA). The apparatus is
shown in Fig. 1.
252 G. Corkidi et al.
Cartographic projections of a mango fruit
To obtain map projections of mango fruits for the quan-
titative evaluation of anthracnose, lesions on the whole
surface of the fruit were measured. The mango fruit basi-
cally has a convex envelope with a predominantly ellipsoi-
dal shape. Its irregular shape does not allow the use of a
simple analytical model. For the purpose of this study, it
is important that the map projection reflects the exact
dimension of the original anthracnose spots, no matter
if their shape is distorted. The map produced gives an
‘equal-area’ projection (Bugayevskiy & Snyder, 1995;
Muehrcke & Muehrcke, 1998; Tobler, 2004).
The simplest and most intuitive way of mapping the
surface of a three-dimensional object would be to use a
cylindrical projection (the surface of the object is mapped
into a cylinder). However, this kind of projection is not of
the equal-area type. Here we describe the implementation
of an equal-area pseudocylindrical projection that takes
into account the three-dimensional irregularities (Stooke,
1998) of each particular fruit, correcting the vertical and
horizontal area deformations due to the inherent curves of
the fruit envelope.
Acquisition of images
The peduncle of the mango was placed in the cavity of the
support (Fig. 1) in order to stabilize the fruit. Care was
taken to align the major axis of the mango to be parallel
with the rotation axis of the stepper motor. Simple visual
positioning of the fruit is sufficient, and can be performed
by observing the fruit at its top and rotating the stepper
motor with the digital potentiometer for focus control of
the joystick.
The fruit is illuminated directly with a 300-W incandes-
cent lamp installed at the left-hand side and behind the TV
camera (Fig. 1). The angle between the lamp axis and the
camera–fruit axis should be at least 30° in order to avoid
reflection of the light source in the camera. A white screen
is placed at the rear of the fruit in order to have a clear,
homogeneous image background permitting simple
edge-detection of the fruit.
The image-acquisition procedure was implemented
using the scope-pro module (written in visual basic)
within the image-pro imaging software. A simple set of
instructions was assembled into a macro command to
rotate the stepper motor supporting the fruit. For each
single rotation degree, an image is acquired and stored.
The images at each rotation angle are saved sequentially
until completion of the whole set of 360 images, forming
the three-dimensional collection. Acquisition time for all
these images (n = 360) is c. 2 min.
Two-dimensional projection of the fruit surface
Because an equal-area projection keeps an undistorted
relationship between the real area of the objects to be
mapped and its projection, the areas of the projected
anthracnose lesions of the infected mango may maintain
an equivalent area to the real anthracnose spots. For
this purpose, a pseudocylindrical projection was imple-
mented. Figure 2 shows a mango fruit, its upper and side
schematic views and its pseudocylindrical projection. Two
pairs of points on these views were analysed, with each
pair of points located in different rings or ‘parallels’ that
cut the mango transversely with respect to its major axis
aligned with the stepper motor (Fig. 2a).
Schematically, points P1 and P2 are located over the 0°
‘meridian’ (initial rotation angle) and points P3 and P4 are
located over the 1° meridian (first rotation increment).
Points P1 and P3 (subindex odd-pair) are located in a
‘parallel’ near the ‘north pole’ of the mango fruit where
its diameter (transverse section) is significantly reduced.
Furthermore, points P2 and P4 (subindex even-pair) are
located over the ‘equator’ of the mango fruit, where the
diameter of its transverse section is maximum.
To trace the projections of the first two points (P1 and
P2 in Fig. 2d), the vertical reference meridian correspond-
ing to 0° is traced (this meridian is aligned with the rota-
tion axis of Fig. 2c). This meridian will be the only vertical
straight line, as all the others will be deformed in order to
correct the projected areas. The vertical position of points
P1 and P2 over this meridian will be determined as a func-
tion of the tangent of the mango surface at those points
(angles β1 and β2 of Fig. 2c). By using this procedure, the
deformation of the curved surface of the mango fruit in
the vertical direction is corrected in the map. Points with
an angle β2 = 0° will be mapped directly without any
vertical correction factor.
To project points P3 and P4, the angular displacement
distances Dw1 and Dw2 must be known. Figure 2(b)
(schematic upper view of fruit) shows how these angular
distances Dw1 and Dw2, swept by points P1 and P2 for a
same rotation angle, are of significantly different magni-
tudes. A classical cylindrical projection does not take
account of this situation, and fixes equal-magnitude
displacement distances for the mapped points; for this
reason, this kind of projection normally has a rectangular
or squared geometry where the objects near the ‘poles’ are
gradually distorted with over-dimensioned areas. This
effect is clearly demonstrated in cylindrical projections of
the Earth’s North and South poles.
As the rotation increments are small (1°), the values of
Dw1 and Dw2 can be approximated to the linear distances:
Dwi = Di × tan α
where Dwi = angular distance; Di = radial distance; and
α = rotating step angle. To solve this equation, Di needs to
be determined. As there is access to the 360 acquired
images of fruit, distances D1 and D2 can be measured
directly in the orthogonal image of the point to be pro-
jected: these distances can be measured directly in the side
view of the fruit at 90° (Fig. 2c).
Anthracnose lesion segmentation
Anthracnose lesions over the pseudocylindrical projec-
tion need to be segmented (contour detection) for area
© 2005 BSPP Plant Pathology (2006) 55, 250–257
 Image analysis of lesions on mango fruit 253

Figure 2 Schematic representation of the projection of selected test points (over 0°, 1° meridians) as an example of the construction of the
pseudocylindrical ‘equal-area’ projection of the three-dimensional surface of a fruit. (a) Frontal view of a mango: points P1 and P3 located at the ‘north
pole’; points P2 and P4 on the ‘equator’. (b) Top view of a mango: points P1 and P2 correspond to initial rotation at 0°; D1 and D2, corresponding radial
distances of current points to vertical axis of mango; Dw1 and Dw2, angular distances. (c) Side view of mango (90°) to measure distances D1 and
D2 and angles β1 and β2 relative to the tangent of the peel. (d) Pseudocylindrical equal-area projection of points P1–P4.

measurement. Highly contrasted lesions (black spots over

clear yellow background) were detected automatically
using an automatic thresholding method (included in the
image-pro plus 4·45 software) as the between-class variance
segmentation method (Otsu, 1979). For this purpose, the
image was converted to grey-level mode. Other less-
contrasted lesions were segmented semi-automatically
using the ‘magic wand trace mode’ (also included in the
imaging software) by which a pixel within the lesion is
seeded manually (preferably near the border of the lesion),
allowing the imaging software to search automatically for Figure 3 Estimation of intrinsic error produced by the system. Black
neighbouring pixels with similar statistical features based labels of known area simulate an infected area in a plastic model
on colour or grey-level value, or until satisfactory contour of a mango fruit. Ten different patterns were evaluated over this
detection. Other segmentation methods can be used, as model. An average error of −0·1%, SD = 0·44 (r 2 = 0·99) was
described by González & Woods (2002). found between known areas and those evaluated by means of the
cartography. (a) Single view of the calibrated mango (plastic model).
(b) Cartography of the whole calibrated mango (reconstructed from
Estimation of error produced by the cartographic 360 views).
system
To evaluate the intrinsic error produced by the carto-
graphic system, the difference was evaluated between a labels of diameter 0·64 and 1·27 cm, Avery Dennison,
known simulated infected area in a mango fruit and that USA), and semirectangular (rounded salient angles)
produced by the system. For this purpose, a plastic model labels 0·9 × 1·3 cm (Tuk-Stik, Mexico), as shown in
of a mango fruit was covered with black, round and/or Fig. 3. Ten different spot patterns were created over the
semirectangular labels of known area (round coding mango models and their respective cartographies. The

© 2005 BSPP Plant Pathology (2006) 55, 250–257

254 G. Corkidi et al.

Figure 4 Effect of Colletotrichum

gloeosporioides inoculum level on affected
area (as percentage of total fruit area) after
5 and 10 days’ storage of mango fruits.
*, No reliable measurements performed as the
infected area was close to 100%. Treatments
with the same superscript are not significantly
different (P = 0·05).

known area of the spot patterns was compared with that

provided by the system. In this way, an average error
of −0·1% (SD = 0·44) and a Pearson’s correlation co-
efficient of r 2 = 0·99 were determined.

Assessment scale based on measured lesion area

Evaluation of the lesion area was carried out as described
above (using cartography of the fruits). As trained experts
will carry out the evaluation in the field, pictures of the
actual fruits, showing the two 180° sides of each mango,
were used to propose the assessment scale based on the
image analysis-measured lesion areas.

Results and discussion

An image-analysis system was developed for the accurate
quantitative measurement of spot-like lesions on diseased
mango fruits. This was obtained by acquiring a sequence
of images of the anthracnose-affected fruit rotating 360°
on its vertical axis, and capture of pseudocylindrical
projections to allow the accurate quantification of the
diseased fruit surface.
The effect of the inoculation level of the pathogen
on the anthracnose lesion area was evaluated after 5 or
10 days’ incubation (Fig. 4). Although actual spore
densities on mangoes were not assessed, significant differ-
ences were found among treatments. After 5 days, the
inoculation made with 105 and 106 conidia mL−1 resulted
in a mean affected area <1%. Significant differences were
found for mangoes inoculated with 107 conidia mL−1,
resulting in a mean affected area close to 7% of the fruit
surface. After 10 days, the mean area affected by anthra-
cnose was 2 and 12% for inocula of 105 and 106 conidia Figure 5 Mean equivalent diameter distributions of anthracnose spots
mL−1, respectively. Fruits inoculated with 107 conidia mL−1 in a sample of 10 mangoes as a function of incubation time.
could not be evaluated as the disease developed rapidly to
almost 100%, preventing mangoes from being supported
in the apparatus. No disease developed in the control with 106 conidia mL−1. Generally, small spots decreased
disinfected fruits. in frequency and the distribution shifted to larger sizes.
Figure 5 shows the mean relative frequency of the size- However, spots with a mean equivalent diameter of
distribution of anthracnose spots changed as function of 1– 4 mm diameter were most abundant throughout this
incubation time (from 4 to 8 days) for 10 fruits inoculated incubation period.

© 2005 BSPP Plant Pathology (2006) 55, 250–257

 Image analysis of lesions on mango fruit
Figure 6 Development of single anthracnose spots on mango fruit as measured by the image-analysis technique.
The image-analysis system followed the evolution of
individual spots over time (Fig. 6). There was no direct
correlation between initial size or position of the spots and
the rate at which they enlarged in diameter.
Figure 7 shows the proposed scale for the hedonic
evaluation of mangoes. The aim of this scale was to pro-
vide a practical and reliable tool for the training of hedonic
evaluators. As a result of the validation of this image-
analysis technique, a large number of illustrations covering
the whole range of anthracnose severity were obtained.
From these, it is possible to select pictures depicting specific
quantitatively measured affected areas. In Fig. 7 each of the
anthracnose categories (in terms of percentage of affected
area) established by Brodrick (1978) have been followed,
using representative mango pictures for each category.
According to the scales of Smoot & Segall (1963) and
Koomen & Jeffries (1993), disease severity is defined
mainly by either size (diameter) or number of spots,
respectively. Nevertheless, it is possible to find some fruits
with many small spots or others with a single large lesion,
and this can present problems in assessing the severity of
disease accurately. Brodrick’s (1978) scale is ‘calibrated’
as a function of a subjective estimation of the percentage
of the surface affected. In contrast, the acquired images
developed here and their respective pseudocylindrical
projections allowed the number of spots and the infected
area to be assessed accurately, and could be used for a
range of other diseases with similar symptomatology.
Furthermore, the use of image analysis allowed the
characterization of every spot (over time) on the surface of
each mango fruit evaluated, which is not possible using
© 2005 BSPP Plant Pathology (2006) 55, 250–257
255
existing qualitative disease assessment criteria. The image-
analysis technique can be used to monitor accurately the
effects of ripening, storage conditions, fungicide or
biological control treatments on fruit that develop symptoms
under postharvest conditions.
Based on the accuracy and usefulness of this technique,
the proposed anthracnose assessment scale based on
Brodrick’s (1978) scale, includes pictures of infected
mangoes falling into a particular category after quan-
titative measurement by the image-analysis technique.
The accuracy of the method developed was determined by
comparing a set of values from different patterns with a
known simulated infected area on a plastic model of a
mango fruit, the values being assessed by the system. A
small error was found. The black labels simulating
the infected area on plastic model fruits have high con-
trast and clear, sharp edges, and a simple automated
contour detection method has therefore provided accu-
rate results. Spots on real fruits do not always have
such good contrast and sharp edges, and this produced
a small error. Nonetheless, the data provided by this re-
evaluation of disease assessment criteria should assist
in training personnel who judge and grade fruit at har-
vest, during storage, and prior to marketing.
The accuracy of the method also depends on the
number of images forming the pseudocylindrical projec-
tion, and the correction performed to compensate for the
distortion required for a 3D irregular surface projected in
a two-dimensional map (Stooke, 1998). In this work, a
maximal rotation resolution of 1° was used to create a
highly accurate projection from 360 images. This means
256
Figure 7 Assessment for field evaluation of severity of mango anthracnose based on experimentally measured percentage of affected area, and
using Brodrick’s (1978) scale.
that each pixel of the fruit can be rescaled, taking into
account the finest irregularities within its surface. If this
resolution is reduced, such correction is not possible for
each pixel. In an extreme case, where no correction is per-
formed in the projection (a simple cylindrical projection),
the measured area of spots near the poles of the fruit may
reach a huge error of up to 100% for β1 = 45° (tangent
angle of the fruit surface; Fig. 2c). However, the resolution
can be adjusted depending on the application of image
analysis and the accuracy required.
Overall, this technique can characterize accurately
the size and number of spots, as well as their distribution
on the fruit. This makes the use of severity indices un-
necessary, as the data on the affected area can be used to
compare quantitatively among treatments and/or condi-
tions. For example, the evaluation of pathogen growth in
terms of spot size (e.g. as a function of storage time) and
the growth dynamics of single spots can be followed accu-
rately. The method also allows quantitative characteriza-
tion of disease development as a function of a variety of
conditions, and in terms of marketing the product. The
technique is relatively easy to implement and can be used
in other plant–parasite interactions in which spots are the
main symptoms of disease.
G. Corkidi et al.
Acknowledgements
The financial support of CONACYT (grant Z-001) and
SAGARPA-CONACYT (grant 2002-C01-0741) is
acknowledged, with thanks. We are grateful to A. Carrillo-
Fasio (CIAD-Culiacán, México) for useful discussions
and for providing mango fruits. We thank M. Patiño-Vera
(Pilot Plant Unit, IBT-UNAM) for technical assistance.
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