Legume Science

ORIGINAL ARTICLE OPEN ACCESS

Prediction of Severe Epidemics of Chickpea Ascochyta

Blight Using Weather Variables
Bita Naseri1 | Farshid Mahmodi2

1PlantProtection Research Department, Kermanshah Agricultural and Natural Resources Research and Education Center, AREEO, Kermanshah,
Iran | 2Dryland Agricultural Research Institute, Sararood Branch, AREEO, Kermanshah, Iran

Correspondence: Bita Naseri ([email protected]; [email protected])

Received: 9 December 2023 | Revised: 20 January 2024 | Accepted: 31 January 2024

Funding: This study was funded by the Iranian Agricultural Research, Education & Extension Organization, project no. 3-­55-­1615-­144-­971442.

Keywords: epidemiology | legumes | multivariate regression | occurrence

ABSTRACT
Chickpea production is threatened by severe epidemics of Ascochyta blight occurring in main chickpea growing lands under ap-
propriate weather conditions worldwide. In this 4-­year research, occurrence of Ascochyta blight was monitored across nine main
chickpea growing areas of Kermanshah province, western part of Iran. Each year, commercial chickpea fields were studied on
a weekly basis from March to June. Disease data were collected as disease incidence (percentage of infected plants) and severity
(percentage of infected tissues) and occurrence of epidemics. Weather data were collected as air temperature, rainfall, and rela-
tive humidity (RH) on a daily basis. According to a factor analysis, which explained 83% of data variance, 13 weather predictors
were selected to estimate disease epidemics developed across different areas. Before modeling, a principal component analysis
determined predictive values for these selected weather variables. Then, eight predictors of rainy days in March and April, mean
RH in February, mean minimum temperature in January–March–April, and rainfalls in May and June were involved in model
based on their predictive values. Current findings advanced our knowledge on the best weather predictors of severe epidemics of
Ascochyta blight in chickpea crops at large scale.

1   |   Introduction two mating types of D. rabiei are present in Kermanshah, sug-

gesting a high potential of the development of severe disease
Chickpea (Cicer arietinum L.) is cultivated in 141,575 lands
epidemics following conducive conditions. Furthermore, 48% of
producing 66,158 tons in Kermanshah Province, Iran
seed samples collected from diverse regions of Kermanshah was
(Anonymous 2022). Chickpea cultivation is threatened by ep-
infected by A. rabiei, with 7% of seed samples showing infec-
idemics of Ascochyta blight (Ascochyta rabiei; teleomorph:
tions greater than 15% (Younesi 1997). In addition, Ascochyta
Didymella rabiei) occurring in this main chickpea producer
blight reduced the number of seeds per pod by 45%, and seed
in Iran. This disease can be highly destructive under appro-
infections averaged within 8%–100% across commercial chick-
priate weather conditions in early planted chickpea fields in
pea fields studied.
March (Younesi et al. 2004). Ascocarps are matured in March,
and then, ascospores are released from the middle of March to Ascochyta blight has been reported as one of the most destruc-
late May under prevailing conditions in Kermanshah. Because tive diseases of chickpea crops worldwide (Pande et al. 2013).
chickpea is commonly planted from late February to late April, In Syria, using tolerant chickpea genotypes followed by twice
ascospore releases are coincided with the emergence of chick- applications of chlorothalonil at seedling and podding stages
pea seedlings in early planted fields (Younesi, Safaee, and showed the best disease management outcomes. Considering
Sheikholeslami 2011). This observation demonstrates that the these Syrian findings, chickpea growers were recommended

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is
properly cited.

© 2024 The Authors. Legume Science published by Wiley Periodicals LLC.

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 26396181, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/leg3.218 by Cochrane Peru, Wiley Online Library on [14/09/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
to early planting of tolerant genotypes, late planting of sus- tested, the discontinuous data for the occurrence of Ascochyta
ceptible genotypes, seed disinfestations by fungicides, and blight were considered for the disease predicting model, 0 = no
application of chlorothalonil at seedling stage (Reddy and evidence of disease, 1 = sparse and low levels of disease occur-
Singh 1990). In Iran, seed disinfestations by carbendazim rence, 2 = severe disease epidemics greater than 40% severity
and chlorothalonil applications have been advised to chick- ratings. This disease predictor was used as dependent variable
pea growers when the disease epidemics develop on tolerant to fit an ordinal logit regression model for predicting severe
genotypes (Younesi and Sheikholeslami 2009). However, epidemics of Ascochyta blight developed in chickpea fields. A
predicting models are still needed to minimize the number factor analysis (FA) was performed on the disease and weather
of fungicide applications in Ascochyta blight epidemics oc- variables using correlation matrix (Naseri and Sharifi 2019).
curred in susceptible genotypes. This assisted with removing less predictive weather variables to
estimate the occurrence of Ascochyta blight epidemics. In the
The predicting model developed by Diekmann (1992) in-
next step, a principal component analysis (PCA) was performed
volved weather variables described in 23 countries from Asia,
on the disease and weather variables (Naseri and Sharifi 2019).
America, and Europe according to a discriminant analysis of
This simplified the selection of most predictive variables to
Ascochyta blight pressure. In Australia, Salam et al. (2011)
model the development of Ascochyta blight epidemics. Those
predicted epidemics of this chickpea disease based on the
principal factors or components with eigenvalues greater than
pathogen inoculum. In Spain, no ascocarp was produced by
1.00 were considered for interpretations. Variables contributed
D. rabiei at temperatures above 10°C and RH lower than 100%
significantly in these considered principal components if their
(Navas-­Cortés, Trapero-­Casas, and Jiménez-­Díaz 1998). In
loading values were greater than 0.35 (Kranz 2003). These
Israel, a 4-­year research predicted the timing of ascocarps' ma-
FA and PCA provided predictive values for 19 and 13 disease
turity according to accumulated degree-­days within 0–15°C
and weather variables, respectively, defined for the current
with more than 10 mm rainfalls (Shtienberg et al. 2005). This
Ascochyta–chickpea pathosystem. Finally, the ordinal logit re-
finding reduced applications of chlorothalonil to 1–2 times
gression model was developed according to those weather pre-
per season. In India, the maximum temperature and RH in
dictors with high contributions in the principal components.
the evening for a period of time from the 9th to 14th week
To evaluate the fitness of regression model, the percentage of
of planting were used to predict Ascochyta blight epidemics
correct predictions of Ascochyta blight epidemics based on the
(Jhorar et al. 1997). However, there is no predicting model spe-
fitted model was determined (Landschoot et al. 2013).
cifically developed for Ascochyta blight epidemics occurring
in Iranian chickpeas. Therefore, this research tried to predict
the occurrence of severe epidemics of this destructive disease
3   |   Results
according to wisely selected weather predictors described in
Kermanshah. Severe disease epidemics mostly with 100% severity ratings oc-
curred during 2017–2018 growing season of chickpea. There
was no disease epidemics developed in chickpea fields during
2   |   Materials and Methods 2018–2019 and 2019–2020 growing seasons. The symptoms of
Ascochyta blight (lower than 40% severity rating) were evident
In this 4-­year research (2017–2021), at least 16 commercial
in chickpea fields across Islamabad, Mahidasht, Sararood,
chickpea fields per year were studied across the nine geographi-
and Sahneh during these two growing seasons. There was
cal regions involving Sarpolzohab and Gilangharb (subtropical),
no disease symptoms observed in commercial chickpea fields
Islamabad and Javanrood (cool temperate), Mahidasht (cool
across all the nine regions studied during 2020–2021 growing
semi-­arid), Sahneh and Ravansar (temperate), and Sararood and
seasons.
Songhor (cold). The local chickpea cultivar, Bivanij, is widely
cultivated in rainfed lands of Kermanshah. In each region, four Although the disease incidence and severity datasets were col-
commercial chickpea fields were selected in random to examine lected for the development of Ascochyta blight in commercial
the occurrence of Ascochyta blight on a weekly basis from late chickpea fields across the nine regions studied, the discontin-
February to early July. The disease incidence was defined as the uous data on the occurrence of Ascochyta blight epidemics (0,
percentage of infected chickpea plants showing symptoms of 1, and 2 levels) were considered for the remainder of statistical
brown to black lesions on aerial parts, dried, and hanged leaves analyses, because this disease variable provided a greater con-
of 20 plants per observation. Five observations were made per tribution in the principal components, which were regarded as
field that resulted in the examination of 100 plants per field. The linear combinations of weather variables (data not shown). Leaf
disease severity was determined as the percentage of infected wetness was ignored in the current research due to the lack of
tissues per plant, assessing five plants per observation. Weather equipment required to record this weather variable.
data involving daily minimum, mean and maximum air tem-
With the help of FA results, the best predictors of Ascochyta
perature, mean daily RH, wind speed, leaf wetness, and daily
blight epidemics among 19 weather variables were determined
rainfalls during winter and spring were obtained from adjacent
(Table 1). The four principal factors of this FA explained 83%
weather stations.
of total variance in Ascochyta blight and weather datasets col-
The other disease datasets were recorded as follows: the disease lected during the four growing seasons of chickpea growth.
onset, occurrence of disease epidemics (0, 1, and 2), and maxi- The first principal factor accounting for 32% of disease-­
mum disease development. Simple correlations between the dis- weather data variance provided moderate loading values for
ease and weather variables were examined for time periods of the number of rainy days and mean RH in April. Mean min-
1–2 weeks and 1, 2, and 3 months. Among the disease variables imum temperatures for January, February, March, and April

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TABLE 1    |    Factor analysis of 19 disease and weather variables linked to Ascochyta blight epidemics occurred during four growing seasons across
nine main chickpea growing regions, Kermanshah.

Principal factors
Weather variables 1 2 3 4
Mean relative humidity in January −0.29 −0.07 0.10 −0.23
Mean minimum temperature in January 0.09 −0.42 0.17 −0.01
Mean relative humidity in February −0.32 −0.00 0.10 −0.42
Mean minimum temperature in February 0.18 −0.35 0.19 −0.16
Rainfall in March −0.25 −0.10 0.18 0.37
No. rainy days in March −0.24 −0.14 0.04 0.56
Mean relative humidity in March −0.30 −0.15 0.13 −0.39
Mean minimum temperature in March 0.13 −0.39 0.12 0.21
Rainfall in April −0.34 −0.07 0.08 −0.07
No. rainy days in April −0.35 −0.02 0.08 0.22
Mean relative humidity in April −0.37 −0.06 0.10 −0.01
Mean minimum temperature in April 0.16 −0.40 0.14 −0.06
Rainfall in May −0.03 −0.21 −0.43 0.00
No. rainy days in May −0.11 −0.20 −0.09 −0.08
Mean relative humidity in May −0.34 −0.18 −0.30 −0.02
Mean minimum temperature in May 0.22 −0.30 0.24 −0.08
Rainfall in June 0.03 −0.12 −0.43 −0.07
No. rainy days in June 0.05 −0.15 −0.43 −0.11
Occurrence of disease epidemics −0.16 −0.29 −0.32 0.12
Eigen values 6.09 4.63 3.88 1.33
Data variance explained 32% 24% 20% 7%
Note: Bold values refer to significant loadings.

significantly contributed in the second factor accounting for component accounting for 27% of variance. Rainfalls in May and
24% of variance. The third principal factor explaining 20% June and the number of rainy days in June corresponded with
of variance provided significant contributions of rainfalls in the third principal component explaining 22% of total variance.
May and June and the number of rainy days in June. Mean Mean RH in February and March and the number of rainy days
RH in February and March and the number of rainy days in and rainfalls in March were linked to the fourth principal com-
March significantly contributed in the fourth principal factor ponent accounting for 9% of data variance. According to the ac-
explaining 7% of data variance. cumulated contributions of variables (Table 2) and the strength
of contributions, the most predictive variables describing appro-
Therefore, the first principal factor defined rainy days and RH in
priate weather conditions for the occurrence of Ascochyta blight
April, the second factor for mean monthly minimum tempera-
epidemics were selected for the regression model.
tures in January–February–March–April, the third factor for
rainfalls in May and June, and the fourth factor for rainfalls and This method of selecting weather predictors based on the FA and
RH in February and March (Table 1). These weather variables PCA results minimized collinearity among variables involved
significantly contributed in the four principal factors were con- in the regression model. Therefore, the ordinal logit regression
sidered for the next statistical analysis. Hence, the 13 weather model was developed to predict Ascochyta blight epidemics oc-
variables were subjected to the PCA to determine their predic- curred in commercial chickpea fields across different geograph-
tive values for developing the ordinal logit regression model. ical areas and weather conditions (Table 3). The current model
explained 92% of variations in the disease and weather variables
The PCA provided predictive values for 13 weather variables
defined during the four growing seasons in chickpea fields stud-
selected for the ordinal logit regression model according to the
ied across the nine regions.
FA results. The four principal components explained 89% of
total variance in the occurrence of Ascochyta blight epidem- The data fitted by the regression model corresponded with the
ics during four growing seasons across nine chickpea growing response data collected from commercial chickpea fields during
regions (Table 2). The first principal component accounting the four growing seasons across the nine regions (Figure 1). In
for 32% of data variance provided moderate loading values for the 2017–2018 seasons with the occurrence of severe Ascochyta
the number of rainy days in April and mean RH in February blight epidemics, the mean minimum temperatures in January,
and April. Mean minimum temperatures in January, March, March, and April were greater than those in the 2020–2021
and April significantly contributed in the second principal without the disease occurrence (Figure 2). The highest levels

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TABLE 2    |    Principal component analysis of 13 Ascochyta blight and weather variables to determine their predictive values.

Principal components Accumulated

Selected variables 1 2 3 4 contributions
Mean minimum temperature in January −0.20 0.42 −0.21 0.07 0.90
Mean relative humidity in February 0.35 0.13 0.06 0.50 1.04
Mean minimum temperature in February −0.27 0.31 −0.27 0.18 —
Rainfalls in March 0.29 0.24 −0.07 −0.35 0.95
Number of rainy days in March 0.22 0.29 0.10 −0.51 1.12
Mean relative humidity in March 0.28 0.29 0.01 0.49 1.07
Mean minimum temperature in March −0.33 0.38 −0.17 −0.19 0.97
Number of rainy days in April 0.38 0.18 0.08 −0.15 0.79
Mean relative humidity in April 0.39 0.23 0.07 0.09 0.78
Mean minimum temperature in April −0.27 0.36 −0.21 0.09 0.93
Rainfalls in May −0.18 0.17 0.47 0.00 0.82
Rainfalls in June −0.20 0.05 0.45 0.06 0.76
Number of rainy days in June −0.24 0.07 0.44 0.11 0.86
Occurrence of disease epidemics −0.03 0.32 0.40 −0.07 0.82
Eigen values 4.40 3.79 3.11 1.22 —
Data variance explained 31.5 27.1 22.2 8.7 89.4
Note: Bold values refer to significant loadings.

TABLE 3    |    Ordinal logit regression model to predict occurrence of Ascochyta blight epidemics in chickpea field according to best weather
predictors.

Predictors Parameter estimate t prob.

Constant 1 2.80 0.013
Constant 2 7.61 0.001
MMT January × MMT March × MMT April 0.01 0.003
MRH February × NRD March × NRD April 0.01 0.001
Rainfall in May × Rainfall in June 0.98 0.001
Abbreviations: MMT = mean monthly minimum temperature; MRH = mean monthly relative humidity; NRD = number of rainy days.

4   |   Discussion
Due to heavy yield losses to Ascochyta blight epidemics in main
chickpea growing regions of Kermanshah, a concise develop-
ment of predicting model is highly needed to optimize timing
of fungicide applications. Thus, it is crucial to determine the
best weather predictors of this destructive disease before the
development of severe epidemics under agro-­ecological con-
ditions in Kermanshah. It is previously known that severe
Ascochyta blight epidemics develop in early planted chickpea
(susceptible cultivar Bivanij) fields in March when ascocarps
are matured and then released from mid-­March to late May
under prevailing conditions in the current study area (Younesi
FIGURE 1    |    Response data correlated to fitted data estimated by
et al. 2004). Moreover, such an availability of the pathogen in-
ordinal logit regression model predicting Ascochyta blight epidemics in
ocula threatens young seedlings of chickpea commonly planted
chickpea fields.
early from late February to late March (Younesi, Safaee, and
Sheikholeslami 2011). An earlier model predicted Ascochyta
blight epidemics according to the mean temperatures, rainy
of rainfalls in spring months, April–May–June, were recorded days, and rainfalls in the first and second months of planting
during the 2017–2018 season (severe disease epidemics oc- chickpea (Diekmann 1992). The weather variables selected in
curred) compared to the lowest rainfalls in the 2020–2021 sea- the present findings are in agreement with this old predicting
son (no epidemic observed; Figure 3). model; however, this research added to the duration of these

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FIGURE 2    |    Mean monthly minimum temperatures recorded in
nine chickpea growing regions studied during four growing seasons. FIGURE 3    |    Monthly rainfalls recorded in nine chickpea growing
regions studied during four growing seasons.

weather data recorded for the 2 months in Diekmann's model. in 2–3 months after planting chickpeas in the study area, in
Hence, our predicting model developed based on the FA and May and June. This may suggest the important role of this
PCA results fitted rainfall, rainy days, and temperature pre- weather predictor in the distribution of infections, plant-­by-­
dictors for a longer period of time, from 1–2 months before plant and field-­by-­f ield. Such noticeable associations of air tem-
planting chickpea to 2–3 months after planting crops. Such re- perature and rainfall with the occurrence of severe epidemics
markable associations of Ascochyta blight development with of Ascochyta blight 1–2 months after planting chickpea may
weather data collected 1–2 months before planting might be support Indian findings. In India, the maximum temperature
attributed to the noticeable impact of weather conditions on and RH in the evening for a period of time from the third to
inocula survival and formation (Navas-­Cortés, Trapero-­Casas, the middle of the fourth month after planting predicted severe
and Jiménez-­Díaz 1998; Salam et al. 2011; Younesi, Safaee, and Ascochyta blight epidemics (Jhorar et al. 1997). Therefore, it ap-
Sheikholeslami 2011). This may explain why the mean mini- pears that predicting the disease epidemics based on the tem-
mum temperature in January (2–3 months before planting) and perature, RH, rainfall, and rainy days for a longer period of time
mean RH in February (1–2 months before planting) were fitted covering 6 months of chickpea growing season justified 92% of
in the present model as effective as the temperature and rainy variability in disease-­weather datasets.
days in the first and second month of planting chickpea crops.
In Australia, Salam et al. (2011) predicted epidemics of chick-
Furthermore, the current findings revealed reasonable predic- pea Ascochyta blight based on the pathogen inoculum and daily
tive values of mean monthly minimum temperature and RH temperature and rainfalls. In Spain, no ascocarp was produced
in order to model the development of Ascochyta blight epidem- by D. rabiei at temperatures above 10°C and RH lower than
ics in chickpeas. Moreover, the variable of rainfall was associ- 100% (Navas-­Cortés, Trapero-­Casas, and Jiménez-­Díaz 1998).
ated with the occurrence of disease epidemics when recorded In Israel, a 4-­year research predicted the timing of ascocarps

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maturity according to accumulated degree-­days within 0–15°C Kranz, J. 2003. “Comparison of Temporal Aspects of Epidemics: The
with more than 10 mm rainfalls (Shtienberg et al. 2005). Disease Progress Curves.” In Comparative Epidemiology of Plant
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these weather predictors. Whereas in India (Jhorar et al. 1997) Landschoot, S., W. Waegeman, K. Audenaert, G. Haesaert, and D. Baets.
and in the current research, weather variables recorded during 2013. “Ordinal Regression Models for Predicting Deoxynivalenol in
a definite period of time were used to predict severe Ascochyta Winter Wheat.” Plant Pathology 62: 1319–1329.
blight epidemics occurring in chickpea crops. This suggested Naseri, B., and F. Sharifi. 2019. “Predicting Wheat Stripe Rust Epidemics
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developed by Diekmann (1992) was used as a basis of modeling “Influence of Relative Humidity and Temperature on Development of
disease epidemics in India (Bal et al. 2008), the current observa- Didymella rabiei in Chickpea Debris.” Plant Pathology 47: 57–66.
tions might also explain why this old model could not predict se- Pande, S., M. Sharma, P. M. Gaur, et al. 2013. “Biplot Analysis of
vere epidemics of chickpea Ascochyta blight in Iran (not shown Genotype × Environment Interactions and Identification of Stable
data). Furthermore, considering the importance of primary in- Sources of Resistance to Ascochyta Blight in Chickpea (Cicer arietinum
ocula in the forms of seed-­borne or stubble-­borne in the sever- L.).” Australasian Plant Pathology 42: 561–571.
ity of Ascochyta blight epidemics (Salam et al. 2011; Shtienberg Reddy, M. V., and K. B. Singh. 1990. “Management of Ascochyta Blight
et al. 2005; Younesi 1997), monitoring weather conditions for of Chickpea Through Integration of Host Plant Tolerance and Foliar
at least 2 months before planting is required depending on the Spraying of Chlorothalonil.” Indian Journal of Plant Protection 18:
65–69.
growing region.
Salam, M. U., J. Galloway, W. J. MacLeod, et al. 2011. “G1
Blackspotmanager Model Predicts the Maturity and Release of as-­
5   |   Conclusion Cospores in Relation to Blackspot Disease of Field Pea.” Australas Plant
Path 40: 621–631.
Therefore, it could be concluded that predicting Ascochyta Shtienberg, D., E. Gamliel-­Atinsky, B. Retig, S. Brener, and A. Dinoor.
blight epidemics based on a further weather descriptors involv- 2005. “Significance of Preventing Primary Infections by Didymella
ing air temperature, RH, rainfall, and rainy days for a longer rabiei and Development of a Model to Estimate the Maturity of
period of time covering 6 months of chickpea growing season Pseudothecia.” Plant Disease 89: 1027–1034.
justified nearly the entire of variability in disease-­weather data- Younesi H. 1997. “Evaluation of Iranian Chickpea (Cicer arietinum)
sets. This improved the predictability of modeling Ascochyta Seeds Infected by Ascochyta Blight and its Distribution in Kermanshah
blight epidemics occurring in chickpeas when compared to the Province,” Iranian Plant Protection Research Institute, Technical re-
earlier models developed in the world as discussed. port no. 77-390, 43.
Younesi, H., S. M. Okhovvat, G. A. Hedjaroude, S. J. Zad, and A.
R. Taleei. 2004. “Evaluation of Chickpea Resistance Against Some
Isolates of Ascochyta rabiei, the Causal Agent of Ascochyta Blight.”
Author Contributions
Communications in Agricultural and Applied Biological Sciences 69:
Bita Naseri: Data curation and analysis; Investigation; Paper writing. 663–665.
Farshid Mahmodi: Data curation; Investigation.
Younesi, H., D. Safaee, and M. Sheikholeslami. 2011. “Phenology
of Didymella rabiei on Chickpea Debris in Kermanshah Province.”
Conflicts of Interest Journal of Plant Pathology 47: 457–464.
The authors declare no conflicts of interest. Younesi, H., and M. Sheikholeslami. 2009. “An Evaluation of the
Effectiveness of some Fungicides in Controlling Chickpea Light
(Kermanshah Province).” Iranian Journal of Plant Protection Science
Data Availability Statement
39: 45–53.
Data produced by this submission are available upon request.

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