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Article

Occurrence Regionalization of Kiwifruit Brown Spot in Sichuan

1
Plant Protection Department, College of Agronomy, Sichuan Agricultural University, Chengdu 611130, China
2
Sichuan Provincial Academy of Natural Resource Sciences, Chengdu 610041, China
*
Author to whom correspondence should be addressed.
J. Fungi 2023, 9(9), 899; https://doi.org/10.3390/jof9090899
Submission received: 31 July 2023 / Revised: 29 August 2023 / Accepted: 29 August 2023 / Published: 31 August 2023
(This article belongs to the Special Issue Modeling, Warning and Management Strategies of Crop Fungal Disease)

Abstract

:
Kiwifruit brown spot caused by Corynespora cassiicola is the most significant fungal disease in Sichuan, resulting in premature defoliation, which had a significant impact on yield and fruit quality. The objective of the study was to determine the occurrence regularity and suitability of kiwifruit brown spot in Sichuan. The occurrence of the disease in the main producing region was continuously monitored, the maximum entropy (MaxEnt) model was used to predict its potential distribution, and the key environmental variables were identified using the jackknife method. The results indicated that kiwifruit brown spot was widely distributed across the entire producing region in Sichuan, predominantly affecting the variety “Hongyang”. The incidence (p < 0.01) and disease index (p < 0.05) showed a significant positive correlation with the cultivar, and decreased with the altitude increasing. The average area under the ROC curve (AUC) of 10 replicates was 0.933 ± 0.012, with an accuracy of 84.44% in a field test, confirming the reliability of the predicted results. The highly suitable distribution areas of kiwifruit brown spot were mainly located in the Chengdu and Ya’an regions. The entire Panzhihua region was an unsuitable distribution area, and the entire Pujiang County and Mingshan District were highly suitable distribution areas. The key environmental variables affecting the potential distribution of kiwifruit brown spot included isothermality (24.3–33.7%), minimum temperature in August (16.3–23.6 °C), maximum temperature in July (25.5–31.2 °C), minimum temperature in June (15.6–20.9 °C), precipitation in August (158–430 mm), and average temperature in October (15.6–18.8 °C). This study provides a theoretical basis for the reasonable layout of the cultivar and the precise prevention and control of the disease.

1. Introduction

Kiwifruit is one of the most popular fruits worldwide due to its special flavor and abundant nutrient contents, especially vitamin C, minerals, and dietary fiber [1,2]. Kiwifruit is a perennial cash crop, which can provide continuous considerable economic benefit to growers [3]. At present, kiwifruit occupies an important position in the international fruit business. In leading producing countries, such as China, New Zealand, and Italy, kiwifruit is the main source of income for local families, making it a vital parameter in their economy [4]. The kiwifruit industry in Sichuan has experienced unprecedented development since 2008, with its current output ranking second in China [5]. Among the cultivated varieties, red-fleshed kiwifruit, especially “Hongyang”, has been widely cultivated, with a planting area reaching 50,000 hectares until 2018. Kiwifruit brown spot caused by Corynespora cassiicola is a fungal airborne disease [6,7], which is the second most significant disease, followed by kiwifruit bacterial canker disease, in Sichuan [8]. The disease spreads rapidly, and the incidence can reach 90% to 100% during the harvest stage. In some orchards, functional leaves are almost entirely lost, leading to the premature sprouting of autumn shoots, and the fruits lose water severely, shrivel, and soften, losing commodity value and causing huge yield loss [8]. With the continuous cultivation of highly susceptible varieties, kiwifruit brown spot has become an escalating concern and a significant limiting factor for industry development. Therefore, understanding the occurrence regularity and distribution regionalization of the disease is of utmost importance.
Previous studies on the epidemic of plant diseases and pests have been limited by technical barriers and other factors, restricting their spatial development to relatively small scales, typically within a confined infected field. However, recent advancements in geographic information system (GIS) technology have enabled the analysis of large-scale spatial data, which makes it possible to regionalize the occurrence and development regularity of diseases and pests in large-scale regions, even on a global scale. Zou et al. [9] regionalized the oversummer range of wheat powdery mildew using the GIS ordinary kriging method combined with the digital elevation model (DEM) of China. Kistner-Thomas et al. [10] assessed the relationship between grasshopper density survey data and 72 biologically relevant GIS-based environmental variables and developed a regression model to predict the mean density of an adult grasshopper from 2012 to 2016. At present, in the research on the suitable regionalization of diseases and pests, correlation analysis, weight coefficient distribution, and assignment of each impact factor are first carried out with mathematical methods; then the comprehensive factors are graded by the index classification method, the data are rasterized by GIS, the value of the vacant area is inserted, and the regionalization results are finally determined [11]. The accuracy of the model primarily relies on the key factors. Accurately understanding occurrence regularity could lay a good foundation for the subsequent distribution regionalization. Peng et al. [12] successfully identified the occurrence and epidemic regularity of wheat stripe rust in Nanchong, achieving 100%, 98%, and 95% accuracy rates for short-term, medium-term, and long-term predictions, respectively. Chen et al. [13] used trajectory analysis and an effective accumulated temperature model to simulate the migration process and development progress of Spodoptera frugiperda, clarifying its migration path and occurrence regionalization in China.
The maximum entropy theory was the most objective criterion for selecting the statistical characteristics of random variables. Based on this theory, the maximum entropy (MaxEnt) model is a quantitative analysis tool, which has been widely applied in plant protection due to its stable operation, simplicity, rapid calculation, and high accuracy [14,15,16]. Zhang et al. [17] collected geographic location information on Prunus salicina and one of the brown rot pathogenic species (Monilinia fructicola), applying the MaxEnt model to simulate their potential suitable distribution in China. Wang et al. [18,19] utilized the MaxEnt model based on distribution information and environmental variables to investigate the suitability of kiwifruit bacterial canker disease in Sichuan and predict its potential distribution under climate change. Evaluating the accuracy of the model is an essential step, accomplished by employing different evaluation methods and standards with effective evaluation indexes. Among these, the area under the receiver operating characteristic (ROC) curve (AUC) has been widely used. Wei et al. [20] used the AUC to evaluate the accuracy of the MaxEnt model in predicting the potential distribution of maize chlorotic mottle virus (MCMV) under historical and future climatic conditions. Cho et al. [21] evaluated the accuracy of spatial (regression kriging) and nonspatial (MaxEnt) models to simulate the distribution of two invasive plant species (Ambrosia artemisiifolia and Ambrosia trifida) by AUC.
Kiwifruit brown spot primarily occurs during high temperature and high humidity seasons, and initially appears in late June and lasts until October. On the other hand, kiwifruit bacterial canker disease is a low-temperature disease, occurring from November to May the following year. Both diseases significantly threaten the healthy development of the kiwifruit industry and substantially impact the variety layout. Meanwhile, their phenological periods and the physiological and biochemical characteristics are completely different. Therefore, the development of this study can provide more scientific and rational guidance for the variety layout of kiwifruit in Sichuan. At present, the occurrence regularity of kiwifruit brown spot in Sichuan has not been clearly elucidated, resulting in blind prevention and control and serious pesticide abuse in production, which is not conducive to the healthy development of the industry. The international scientific community has dedicated many efforts to enhancing resilience and sustainability in agriculture, with a particular emphasis on reducing pesticides [22], including in kiwifruit cultivation [23,24]. Disease prediction is a prerequisite for disease management and plays an important role in integrated pest management [25]. The database established based on long-term monitoring is the foundation for an accurate disease prediction [26]. Early preparation for prevention can not only improve the effectiveness and benefits, but also reduce unnecessary costs and environmental pollution caused by pesticide abuse [27]. Moreover, studies on kiwifruit brown spot are still in the initial stage and mainly focus on pathogen identification, population diversity, resistance of cultivars, and disease control method [3,6,7,28]. However, a suitable regionalization based on climate conditions remains unknown, warranting further study.
In this study, the epidemic of kiwifruit brown spot in the main producing region was monitored over the long term, and the potential distribution of this disease in Sichuan was employed to predict it using the MaxEnt model. The objectives of this study were to (1) clarify the disease occurrence regularity to provide rational guidance for the variety layout; (2) to evaluate the key environmental variables affecting the distribution of this disease; (3) to determine the suitability of this disease in Sichuan, aiming to provide a theoretical basis for the prediction, precise prevention, and control of the disease.

2. Materials and Methods

2.1. Sources of Software and Map

MaxEnt software (version 3.4.1) was downloaded from the Museum of Natural History (https://biodiversityinformatics.amnh.org/open_source/maxent/, accessed on 29 November 2022), Java software was downloaded from its official website (https://www.oracle.com/java/, accessed on 31 July 2022), ArcGIS software (version 10.8.1) was downloaded from the ESRI website (https://support.esri.com/en/Products/Desktop/arcgisdesktop/arcmap, accessed on 1 December 2022), and the base map was provided by the National Meteorological Information Centre of China.

2.2. Determination of the Occurrence of Kiwifruit Brown Spot

During 2012–2022, the occurrence and distribution of kiwifruit brown spot in the main production regions in Sichuan were continuously assessed. Detailed geographical information (longitude, latitude, and altitude), cultivar, and disease occurrence were recorded. The assessment involved six prefecture-level administrative regions, including Chengdu, Ya’an, Guangyuan, Deyang, Mianyang, and Meishan, and was conducted at the end of the disease logistic phase, namely, mid- to late September.

2.3. Measurement of Disease Severity

Each experimental site consisted of five plots, with three trees per plot, totaling fifteen trees. Each tree was examined from five directions (east, west, south, north, and middle), with two branches per direction. From each branch, five leaves were selected, starting from the base upwards, resulting in a total of fifty leaves per tree. The standard of classification for disease severity is presented in Table 1. The disease index (DI) was calculated according to the following formula [3]. The disease level was divided into three categories [8]: high (DI ≥ 66.67), moderate (33.33 ≤ DI < 66.67), and low (0 < DI < 33.33).
D I = ( t h e   l e a v e s n u m b e r   o f   e a c h   s e v e r i t y × s e v e r i t y ) t h e   n u m b e r   o f   l e a v e s × t h e   h i g h e s t   s e v e r i t y × 100

2.4. Correlation Analysis

The Pearson correlation between variety and disease index was determined by SPSS 21.0. The altitude and disease index of the “Hongyang” variety were extracted for correlation analysis.

2.5. Acquisition and Processing of Distribution Information

Kiwifruit brown spot disease primarily occurred in red-fleshed kiwifruit, widely cultivated in Sichuan. It has also been reported in Guangxi, Hubei, and Chongqing, exhibiting strong regional characteristics. Therefore, the other distribution information was mainly obtained by searching published papers [3,7,28], inquiring the kiwifruit disease and pest prediction and forecast reports issued by local plant protection stations and agricultural technology and meteorological cooperative service reports, and consulting local plant protection staff. Through the above procedure, 108 occurrence records were evaluated. By incorporating the 122 available experimental sites collected during the initial stages, a total of 230 distribution points were obtained.
The distribution points with specific information were directly applied, while those lacking latitude and longitude were inquired in the global geographic information integrated database GeoName and the Baidu coordinate picking system to extract the coordinate information. The buffering area analysis function of ArcGIS was used to calculate the distance between the grid center and distribution points. Only the closest record to the center was retained within the same grid. The above distribution records in the order of species, longitude, and latitude were imported into Excel, with a positive north latitude and east longitude and a negative south latitude and west longitude. After the screening process, 225 valid points were retained for constructing the models (Figure 1), and the species distribution information was transferred to the CSV file required by MaxEnt.

2.6. Acquisition and Processing of Environmental Variables

All environmental data were obtained for free from the WorldClim database (http://www.worldclim.org/, accessed on 28 August 2023), which provides interpolated raster data based on global meteorological record information. The above data were in TIFF format with a spatial resolution of 2.5 arc-minutes, including 67 environmental variables, among which were 19 bioclimatic factors, monthly mean precipitation, monthly mean temperature, maximum and minimum temperature, and other bioclimatic indices (Table 2). The environmental variables were extracted from the administrative zoning map of Sichuan as the base map. The TIFF format was transferred to the ASCII format required by MaxEnt using the format conversion function of ArcGIS. Initially, 67 environmental variables were extracted to build an initial model. The contribution rates and importance of environmental variables were determined by the jackknife method, and those rates of less than 1% were eliminated. The attribute values of environmental variables at 225 distribution points were extracted using the extraction analysis tool of ArcGIS. Pearson correlations between environmental variables were calculated using SPSS 21.0. Variables with a strong correlation were removed, and the relationship between kiwifruit brown spot and meteorological factors was considered to finally screen out variables.

2.7. Construction and Evaluation of MaxEnt Model

The distribution information of kiwifruit brown spot and environmental variables were imported into MaxEnt, and the climate response curve was created to analyze the relationship between each environmental variable and the distribution probability. The prediction map was drawn, and the importance of environmental variables was measured using the jackknife method. The random test percentage was set to 25% and repeated 10 times. The default values of the model were selected for other parameters, and the output path was set for modeling. In this study, AUC was used to evaluate the accuracy of the model simulation. The AUC value ranges from 0.5 to 1, with values closer to 1 indicating a stronger correlation between environmental variables and species distribution and a higher model accuracy. The evaluation criterion is 0.5 ≤ AUC < 0.6, fail; 0.6 ≤ AUC < 0.7, poor; 0.7 ≤ AUC < 0.8, general; 0.8 ≤ AUC < 0.9, good; AUC ≥ 0.9, excellent.

2.8. Geographic Division of Suitability

The ASCII format files output by MaxEnt were transferred to raster format files using the format conversion function of ArcGIS. The potential distribution map of kiwifruit brown spot was extracted from the administrative zone map of Sichuan as the base map, and then the spatial analysis tool was used for reclassification. According to previous studies [29,30], the suitable area was divided into four categories, displaying them in different colors: highly suitable area (p > 0.66, red), moderately suitable area (0.33 < p ≤ 0.66, orange), lowly suitable area (0.05 < p ≤ 0.33, yellow), and unsuitable area (p ≤ 0.05, white). The distribution area of each region and district (county) was calculated using the statistical analysis function of ArcGIS.

2.9. Field Evaluation of the Model

A field test of species distribution was conducted as the most direct and reliable method for model validation. In order to further verify the accuracy of the simulation results, additional 45 actual occurrence records from supplementary determination were introduced for the field test. The actual distribution points were mapped onto the reclassified map, and the corresponding suitable levels were extracted by ArcGIS, and then compared with the actual level of disease occurrence. Both are equally regarded as accurate.

3. Results

3.1. Occurrence of Kiwifruit Brown Spot

A long-term monitoring of the epidemic of kiwifruit brown spot in the main production region revealed that the disease was widely distributed and seriously occurred in all regions (Table 3). Out of 122 investigation sites in the province, 83 sites (68.03%) exhibited a high occurrence level. The disease occurrence was particularly severe in the main cultivated variety, ‘Hongyang’, and the damage was serious, with an average incidence of 92.87% and a disease index of 81.99. Among them, the occurrence in the Chengdu region was particularly severe, with the incidence and disease index reaching 97.15% and 91.96 respectively. Apart from ‘Hongyang’, the disease also occurred commonly in other red-fleshed varieties, such as ‘Donghong’, with an incidence of 83.63%, but the severity was relatively low, with a disease index of 31.08. The disease occurrences in yellow-fleshed varieties, such as Jinyan and Jinshi, and green-fleshed varieties, such as Hayward, Cuiyu, and Actinidia arguta varieties, were relatively low. Pearson correlation analysis showed a significant positive correlation between the incidence and disease index with the cultivar, with the correlation coefficient reaching 0.929 (p = 0.002 < 0.01) and 0.795 (p = 0.033 < 0.05), respectively (Table 4). The correlation analysis between the occurrence and altitude in the ‘Hongyang’ variety showed that the incidence and disease index were significantly negatively correlated with altitude, with the correlation coefficient reaching −0.780 (p = 0.000 < 0.01) and −0.604 (p = 0.000 < 0.01), respectively. The incidence and disease index decreased with the increase in altitude.

3.2. Screening of Environmental Variable

The initial model was constructed using 67 environmental variables (Table 2), with an AUC value of 0.930. The contribution rate of each variable to the model was calculated, and variables with a contribution rate of less than 1% were excluded through the jackknife test. This process resulted in the selection of 11 variables, including bio3, tmin8, tmin6, prec8, tmax7, prec2, prec4, tavg10, bio2, tmin7, and prec6, with a cumulative contribution rate of 93.2% (Table 5). Pearson correlation analysis among environmental variables revealed high correlations between bio2 and bio3 (correlation coefficient: 0.924) and between tmin7 and tavg10, tmax7, tmin6, and tmin8 (correlation coefficients: 0.924, 0.983, 0.983, and 0.996, respectively), all exceeding 0.90 (Table 6). There will be some problems, such as autocorrelation and multiple linear repetition, and redundant information will be introduced in the process of modeling, which will have an impact on prediction accuracy. To eliminate collinearity between variables and avoid overfitting in the simulation process, bio2 and tmin7 were eliminated. Based on the biological characteristics of kiwifruit brown spot, prec2 was eliminated for low biological significance. In summary, 8 variables, including bio3, prec4, prec6, prec8, tavg10, tmax7, tmin6, and tmin8, were selected to construct the final model.

3.3. Suitability Test of MaxEnt Model

ROC curve analysis of the geographical distribution of kiwifruit brown spot using the MaxEnt model showed that the average AUC value of 10 replicates was 0.933 ± 0.012 (Figure 2), which was significantly higher than the random predicted value of 0.5. According to the evaluation criteria, the accuracy of the model was ‘excellent’. The above results demonstrated that the model had high reliability and could be used for subsequent analysis.

3.4. Selection of the Key Environmental Factors

The importance of each variable in the final model was determined by examining the regularized training gains when ‘with only variable’, ‘without variable’, and ‘with all variables’ were used for the simulation. As shown in Figure 3, bio3 was identified as the most important factor affecting the distribution of kiwifruit brown spot, and its training gain reached 1.8. tmin8, tmax7, and tmin6 were also important factors, and their individual training gains exceeded 1.7. prec8 and tavg10 were also important for the disease distribution, with training gains of 1.60 and 1.56, respectively. The contribution of prec6 to the model was the lowest. In conclusion, bio3, tmin8, tmax7, tmin6, prec8, and tavg10 were the key environmental factors affecting the distribution of kiwifruit brown spot.

3.5. Analysis of Response Curve

Figure 4 was displays the response curves between the distribution probability and environmental variables, with a probability of 0.33 as the threshold for dividing the suitability of each variable. The results showed that when the suitable range of bio3 was 24.3–33.7%, the distribution probability exceeded 0.33 and reached its highest value at 29.8%, indicating that it was most conducive to the occurrence of kiwifruit brown spot. Low temperatures in August were not conducive to disease occurrence. When tmin8 was below 16.3 °C or above 23.6 °C, the distribution probability was lower than 0.33 and reached its highest value at 20.2 °C. At 22.7–23.1 °C, the probability fluctuated and reached a small peak at 23.0 °C. High temperatures in July were also unfavorable for disease occurrence. When the range of tmax7 was 25.5–29.1 °C, the distribution probability increased with the temperature increasing, and decreased with the temperature increasing at 29.1–31.2 °C. When the range of tmin6 was 15.6–18.8 °C, the distribution probability increased with the temperature increasing, and decreased rapidly at 18.8–20.9 °C. prec8 exceeding 158 mm indicated a rapid occurrence and epidemic of kiwifruit brown spot. The distribution probability reached the highest at 331 and 430 mm, with no further changes when the precipitation exceeded 430 mm. The suitable range of tavg10 was 15.6–18.8 °C, with the peak value at 16.2 °C.

3.6. Prediction of Potential Distribution

According to Figure 5 and Table 7, the highly suitable areas of kiwifruit brown spot in Sichuan were mainly located in the eastern part of the Chengdu region, the central part of the Ya’an region, the southern part of the Yibin region, the central part of Leshan region, and the eastern part of Meishan region, with a total area of 21,849.83 km2, accounting for 4.49% of the area of the provincial territory. Among them, the Chengdu and Ya’an regions had the highest proportion of highly suitable areas, with 28.12% and 20.94%, respectively. There were no highly suitable areas in the Dazhou, Ganzi, Guang’an, Nanchong, Neijiang, Panzhihua, Suining, Ziyang, and Zigong regions and no moderately suitable areas in the Guang’an, Panzhihua, Suining, and Ziyang regions. Lowly suitable areas were widely distributed in the whole province, except for the Panzhihua region. The entire Ziyang region was classified as lowly suitable areas. The largest area was occupied by unsuitable areas, reaching 318,185.83 km2, mainly distributed in the Ganzi, Aba, and Liangshan regions, with the Ganzi region accounting for the largest proportion, nearly 50%. The entire Panzhihua region was classified as unsuitable areas.
According to Figure 6 and Table 8, highly suitable areas were distributed in all eleven central planting areas of kiwifruit. Except for the Anzhou District and Cangxi County, other regions had highly suitable areas accounting for the largest proportion of their total areas. Moreover, the highly suitable area of Qionglai City was the largest, reaching 1348.75 km2. More than 90% of the total area in Pujiang County, Qionglai City, Mingshan District, and Yucheng District were classified as highly suitable areas. Among them, Pujiang County and Mingshan District were entirely classified as highly suitable areas. The whole area of the Anzhou District and Cangxi County were mainly moderately suitable areas, accounting for 65.15% and 82.31%, respectively. Mianzhu City had the largest lowly and unsuitable areas in among the eleven regions, covering 197.82 and 261.45 km2, respectively.

3.7. Field Test of the Model

Out of the 45 test points, 38 of them were accurately simulated (Table 9). The model accuracy calculated was 84.44%, demonstrating high reliability. Among the 7 inaccurate simulation points, all were overfitted, indicating that the level of the predicted suitability was higher than the actual occurrence.

4. Discussion

In this study, continuous monitoring of the epidemic of kiwifruit brown spot in Sichuan revealed that the occurrence of the disease was more severe in the red-fleshed varieties and less severe in the yellow-fleshed and green-fleshed varieties. These findings were consistent with the resistance evaluation of Huang et al. [28] in the kiwifruit germplasm materials to kiwifruit brown spot. The study also highlighted the close relationship between variety layout and the occurrence and epidemic of kiwifruit brown spot. With the continuous expansion of the highly susceptible variety cultivation, kiwifruit brown spot has become the most significant fungal disease in the Sichuan-producing region. However, the impact of variety simplification becomes increasingly evident, and has led to an increased risk of disaster caused by the disease. At present, the prevention of the disease in production is still mainly dependent on chemical control, which is not conducive to the healthy and sustainable development of the kiwifruit industry. The breeding and utilization of resistant varieties are recommended as the most economical and effective measures to control the disease. Therefore, in highly suitable areas, the introduction of resistant varieties, such as Ruiyu and Jinyan, should be recommended. Additionally, the “technical regulations for comprehensive control of kiwifruit brown spot” [31] formulated by Sichuan Agricultural University should be adopted for the scientific and efficient control of the disease. Consistent with the research conclusion of Cui [32], the incidence and disease index were significantly negatively correlated with altitude; as the altitude increased, they decreased gradually. However, further research is needed to determine the altitude boundary for disease occurrence. Since WorldClim datasets are generated by integrating and interpolating the basic data of meteorological stations at different altitudes around the world, altitude information has been implied [18]. Therefore, altitude was not selected as an environmental variable for the MaxEnt prediction model in this study.
Currently, there is limited information on the occurrence and epidemic regularity of kiwifruit brown spot in large-scale areas. Our group has conducted some work on the epidemic dynamics in the early stage, mainly focusing on field disease monitoring and data collection, providing a certain foundation for the construction of prediction models. In this study, the MaxEnt model was employed to simulate and predict the potential distribution of kiwifruit brown spot in Sichuan, and suitability regionalization was conducted using ArcGIS. The suitable areas of each region were calculated, the distribution of central planting areas was analyzed, and the accuracy of the model was verified through field tests. The results indicated that the highly suitable areas of kiwifruit brown spot were mainly located in the Chengdu and Ya’an regions, while the unsuitable areas were mainly distributed in the Ganzi, Aba, and Liangshan regions. The Panzhihua region was entirely classified as an unsuitable area. According to the central planting areas of red-fleshed kiwifruit, Pujiang County and Mingshan District were entirely classified as highly suitable distribution areas. Both kiwifruit brown spot and bacterial canker disease had an adverse impact on the healthy development of the industry. Therefore, in the layout of varieties, both diseases should be comprehensively considered. Ma. [33] demonstrated that the potential severe and suitable areas for kiwifruit bacterial canker disease were mainly distributed along the Longmen Mountains from south to north, connected with the Qinba Mountains, and concentrated in the Ya’an, Chengdu, and Guangyuan regions, which had a high contact ratio with the highly suitable areas for kiwifruit brown spot in this study. Wang et al. [18] indicated that the unsuitable areas of kiwifruit bacterial canker disease in Sichuan were mainly located in the Ganzi, Liangshan, and Panzhihua regions, consistent with the findings of kiwifruit brown spot in this study. The occurrence regionalization of kiwifruit brown spot in Sichuan has been clarified, which not only provided a scientific and effective theoretical basis for the formulation of a prevention and control strategy, but also played an important role in the layout and development of the kiwifruit industry in combination with previous studies on kiwifruit bacterial canker disease.
A disease epidemic is a result of the interaction between host plants and pathogens under the influence of environmental conditions. Environmental conditions mainly include meteorological factors, soil conditions, tillage system, and cultivation measures, with meteorological factors playing an extremely important role. Many researchers have utilized modeling to select key meteorological factors for disease prediction. For instance, Chen et al. [34] found that the amount of rainfall in spring significantly influenced the date of the grapevine downy mildew symptom onset. Chaulagain et al. [35] used correlation analysis and stepwise logistic regression to identify afternoon humid thermal ratio (AHTR), temperature-based duration variables, and their interaction terms as the most significant variables associated with brown rust epidemics of sugarcane in Florida. Kiwifruit brown spot initially occurred in late June, rapidly spread in mid-July, and gradually slowed down until the end of October. In this study, the key environmental variables affecting the potential distribution were identified using the jackknife method, including bio3, tmin8, tmax7, tmin6, prec8, and tavg10, which completely coincide with the actual phenology period of kiwifruit brown spot. Additionally, kiwifruit brown spot develops rapidly under high temperature and humidity conditions, with excessive temperatures inhibiting its development [3,7], which is consistent with the response curve results that the temperature in June and August should not be too low, the temperature in July should not be too high, and the precipitation in August reaches a certain amount. Although our study did not include all factors contributing to the distribution, the selected environmental variables can provide a basis for the future refinement and assessment of a prediction model of kiwifruit brown spot.
An ecological niche model is an emerging technology based on ecological principles, according to the known geographical distribution information of species and corresponding environmental variables, using specific algorithms to calculate the niche demand of target species in the designated area and combining GIS technology to project its distribution probability onto the map [36,37]. However, species distribution models usually lead to overestimating or underestimating the species distribution, namely, false positive and false negative. In this study, the suitability levels predicted by the MaxEnt model were often higher than the actual disease occurrence level, resulting in many false positives. We supposed that the reason for this phenomenon might be attributed to the species distribution model only distinguishing “existence” or “nonexistence” when extracting distribution information, without considering the disease occurrence level, resulting in overfitting. Additionally, the distribution information in this study was mainly obtained through field investigations and local reports inquiry, with a total of 225 distribution points. The data were true, reliable, and relatively systematic, but there might be some omissions in their completeness, which might also cause some errors. Furthermore, previous studies have indicated that the occurrence and epidemic of leaf spot disease were not only affected by meteorological factors, altitude, and cultivars, but also closely related to abiotic factors, such as planting density, site conditions, and canopy density [14,38,39]. Gonzalez-Dominguez et al. [40] developed a model using weather and host phenology to predict the infection period and disease progression of Phomopsis cane and leaf spot throughout the season, and validated its performance using ROC analysis (AUROC > 0.7). Ortega-Acosta et al. [41] established a Weibull model using multiple abiotic factors to describe the epidemic dynamics of Roselle leaf and calyx spot induced by C. cassiicola. Therefore, various factors should be considered comprehensively in future research to further improve the prediction model of kiwifruit brown spot.

5. Conclusions

In this study, the correlation between the occurrence of kiwifruit brown spot and variety and altitude was revealed, its potential distribution was predicted, and the suitable areas were regionalized, which could provide scientific suggestions for the variety layout of kiwifruit in Sichuan. At the same time, six key environmental variables were identified, which could lay the foundation for the subsequent disease prediction and forecast, and provide a theoretical basis for the precise prevention and control of kiwifruit brown spot.

Author Contributions

Y.Z.: conceptualization, methodology, formal analysis, investigation, writing—original draft, visualization. K.Y.: software, validation, investigation, writing—reviewing and editing. M.M.: methodology, writing—reviewing and editing, supervision. Y.C.: investigation, data curation. J.X.: investigation, data curation. W.C.: investigation, data curation. R.Y.: software, investigation. C.W.: investigation. G.G.: validation, resources, writing—reviewing and editing, supervision, project administration, funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Key R&D Projects of Sichuan Science and Technology Plan (grant numbers 2021YFN0120, 2021YFN0026) (G.G.), Key R&D Projects of Chengdu Science and Technology Innovation Plan (grant number 2022-YF05-01151-SN) (G.G.), and Sichuan Innovational Team of Industry Technology System of Modern Agriculture (grant number sccxtd-2023-02) (G.G.).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We would like to thank Wang, R. L., at the Sichuan Provincial Rural Economic Information Center and Chen, L., at Sichuan Agricultural University for their technical guidance on the MaxEnt model.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Figure 1. Sample distribution points of kiwifruit brown spot.
Figure 1. Sample distribution points of kiwifruit brown spot.
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Figure 2. ROC curve analysis and AUC values for the MaxEnt model.
Figure 2. ROC curve analysis and AUC values for the MaxEnt model.
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Figure 3. Jackknife test for the importance of environmental variables in the suitability distribution.
Figure 3. Jackknife test for the importance of environmental variables in the suitability distribution.
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Figure 4. Response curve between distribution probability and environmental variables.
Figure 4. Response curve between distribution probability and environmental variables.
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Figure 5. Prediction of the potential distribution of kiwifruit brown spot in Sichuan (city boundary).
Figure 5. Prediction of the potential distribution of kiwifruit brown spot in Sichuan (city boundary).
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Figure 6. Prediction of the potential distribution of kiwifruit brown spot in Sichuan (country boundary).
Figure 6. Prediction of the potential distribution of kiwifruit brown spot in Sichuan (country boundary).
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Table 1. The standard of classification for kiwifruit brown spot.
Table 1. The standard of classification for kiwifruit brown spot.
SeverityClassification
0No visible symptoms
1The spots account for 1–5% of the whole leaf
3The spots account for 6–25% of the whole leaf
5The spots account for 26–50% of the whole leaf
7The spots account for 51–75% of the whole leaf
9The spots account for above 75% of the whole leaf
Table 2. Bioclimatic factors used in the initial model.
Table 2. Bioclimatic factors used in the initial model.
VariablesDescriptionsUnits
bio1annual mean temperature°C
bio2monthly mean diurnal temperature°C
bio3isothermality%
bio4standard deviation of seasonal temperature°C
bio5max temperature of warmest month°C
bio6min temperature of coldest month°C
bio7mean temperature annual range°C
bio8mean temperature of wettest quarter°C
bio9mean temperature of driest quarter°C
bio10mean temperature of warmest quarter°C
bio11mean temperature of coldest quarter°C
bio12annual precipitationmm
bio13precipitation of wettest monthmm
bio14precipitation of driest monthmm
bio15precipitation variation coefficient%
bio16precipitation of wettest quartermm
bio17precipitation of driest quartermm
bio18precipitation of warmest quartermm
bio19precipitation of coldest quartermm
precprecipitation of each monthmm
tavgaverage temperature of each month°C
tminmin temperature of each month°C
tmaxmax temperature of each month°C
Table 3. Survey information of kiwifruit brown spot.
Table 3. Survey information of kiwifruit brown spot.
RegionCountyTownLongitude (E)Latitude (N)Altitude (m)VarietiesIncidence Rate (%)Disease
Index
Occurrence
Level
ChengduDujiangyanJuyuan103.71819930.882004648Hongyang100.0099.45High
103.69092330.923192624Hongyang100.0099.37High
103.68573430.957274640Hongyang100.0099.36High
Tianma103.72413731.019014622Hongyang100.0099.19High
103.73720331.014943712Hongyang99.4798.39High
103.71097730.997566628Hongyang99.7399.17High
103.71103830.997706622Hongyang100.0099.75High
103.71721331.025650646Hongyang99.8799.24High
103.73569231.026519619Hongyang100.00100.00High
103.73766731.026325687Hongyang100.0099.13High
103.60915430.988223636Hongyang100.0099.01High
103.76773830.977838618Hongyang100.00100.00High
Puyang103.67602931.062330710Hongyang99.0797.68High
103.71418931.1449671059Hongyang96.8079.81High
103.67907731.031806608Hongyang100.0096.99High
Shiyang103.63925430.888781618Hongyang100.0096.84High
103.64926230.870515604Hongyang100.0098.36High
Yutang103.61904030.970404733Hongyang99.3396.04High
Qingchengshan103.60132430.905453672Hayward21.732.41Low
103.59566030.859226601Hongyang98.4094.13High
Xingfu103.67804530.970588644Hongyang93.4778.92High
Longchi103.55279231.057788912Hayward10.401.16Low
103.66411731.1192421234Hayward8.400.93Low
PujiangDaxing103.42585030.247561602Hongyang100.00100.00High
Ganxi103.36166430.263327597Hongyang100.00100.00High
Chengjia103.40264630.192967500Hongyang/Jinyan97.73/17.6096.76/1.96High
Dating103.39648930.289953593Hongyang100.00100.00High
Xilai103.51050030.304396530Hongyang100.00100.00High
QionglaiGuyi103.58887630.390417479Hongyang100.0096.69High
Huojing103.23081430.3567881400Hongyang77.2068.73High
Pingle103.35836730.383795547Hongyang97.8795.88High
Sangyuan103.40084830.546483622Hongyang98.8094.06High
Yangan103.68541930.401639470Hongyang100.0097.78High
Datong103.22180830.4786821200Hongyang84.2773.88High
Wenjun103.47665630.374584524Donghong92.4047.69Moderate
PengzhouLichun103.89725331.006937653Hongyang94.5390.21High
Guihua103.78250431.102041830Hongyang91.0783.45High
Longmenshan103.81455331.2607371414Hongyang84.1347.34Moderate
Bailu103.91908331.1957171128Hongyang93.8786.62High
Tongji103.83754231.158838886Hongyang96.9389.17High
Gexianshan103.96642731.113843611Hongyang93.7392.13High
XinjinXingyi103.82571330.456078200Hongyang96.5362.68Moderate
Huaqiao103.86946530.431029462Hongyang87.6060.55Moderate
DayiXinchang103.45182730.525427561Hongyang98.9396.90High
Wangsi103.52129330.527021521Hongyang100.0097.34High
Yuelai103.44264330.631438640Hongyang98.4094.13High
Anren103.59084930.467129494Hongyang99.7399.01High
Ya’anYuchengShangli103.03911130.158470889Hongyang91.4787.05High
103.02752130.163007906Yidun19.472.65Low
Bifengxia103.01849830.109764984Hongyang91.6072.16High
Caoba103.14085729.996113600A. arguta12.931.44Low
Duoying102.91658030.020083754 3.730.41Low
Daxing102.98677529.954752688Hongyang93.8787.01High
Babu102.90921629.883380600A. arguta9.201.02Low
MingshanYongxing103.15885730.042103596Hongyang100.0096.99High
103.14394730.049887549Hongshi52.807.01Low
Jianshan103.11747530.157528766Hongyang99.2096.93High
Mengdingshan103.07223930.108014774Donghong94.1327.12Low
Maling103.32431730.129206684Hongyang100.0094.62High
Maohe103.36916830.219322600Hongyang97.7390.33High
Heizhu103.24572030.247830670Gold 36.800.76Low
Zhongfeng103.18112930.188253756Hongyang95.2090.92High
Mengyang103.11636530.114172701Hongyang93.0791.57High
Wangu103.12837730.170035674Hongyang93.4788.38High
103.13734930.185314679Hongyang91.7393.66High
103.13027430.141192890Hongyang91.0788.67High
Baizhan103.31193730.188603624Hongyang85.7387.30High
103.26184230.191358681Hongyang70.5364.56High
YingjingWuxianxiang102.84518329.780242936Hongyang89.2067.01High
Huatan102.78662329.778432935Hongyang84.6766.83High
102.78081129.783500875Hongyang91.7374.12High
Yandao102.85064529.820925894Hongyang90.2773.93High
Qinglong102.86885129.769872722Hongyang94.2775.60High
102.88125929.7732781529Hongyang70.1367.24High
Anjing102.76154529.737654868Hongyang89.7351.91Moderate
Longcanggou102.84698329.707985909Hongyang89.2048.90Moderate
Siping102.66953229.7801591066Cuiyu14.401.60Low
Baofeng102.82639229.863237949Hongyang85.4771.54High
Xintian102.85683229.828373894 7.070.79Low
LushanFeixianguan102.91515030.093092666Hongyang100.0097.02High
Luyang102.96000530.157746965Hongyang85.0771.39High
Siyan102.91036430.142439642Hongyang99.2095.27High
Longmen103.02552430.260615630Hongyang97.2089.32High
ShimianMeiluo102.43811729.3154731335Jinyan13.731.53Low
Yingzheng102.41557429.2749781388Hongyang87.0769.59High
102.41149229.2777061420Hongyang80.6767.90High
102.41071229.2719691369Hongyang78.2768.19High
Xinmin102.19594329.4124361519Hongyang86.6765.34Moderate
Xieluo102.18067729.2197551243Hongyang84.4069.13high
102.18268729.2119211294Hongyang78.1344.44Moderate
102.25503729.2131121585Hongyang76.8039.81Moderate
Caoke102.12280929.4042041357Hongyang72.9338.93Moderate
102.08668829.3902561538Hongshi 257.4710.83Low
Anshunchang102.28415129.2596681240Hongyang82.9369.99High
BaoxingDaxi102.94334230.553705741Hongyang93.8663.88Moderate
Muping102.80347130.347224869Hongyang86.5359.54Moderate
Longdong102.67943230.4643221258Hongyang78.4045.44Moderate
102.72049330.4948491758Hongyang66.2641.50Moderate
GuangyuanCangxiDongxi106.28283432.044742749Hongyang97.0794.15High
Longshan106.33254331.885837630Hongyang94.8080.47High
Yuedong106.23929331.959870700Hongyang87.4778.68High
Yuanba106.09034231.860973400Hongyang96.2762.83Moderate
Qiping106.13257831.898718430Hongyang92.8059.75Moderate
Wenchang106.36368331.987743655Hongyang94.6777.50High
Lingjiang105.96036631.750199400Hongyang93.7366.12Moderate
Longwang105.98280931.984019650Hongyang91.6079.81High
ZhaohuaWeizi105.89586032.174634709Hongyang93.0792.09High
Yuanba105.97351432.329941597Hongyang97.2094.62High
Zhaohua105.72369232.337770626Hongyang90.5366.34Moderate
DeyangShifangJiandi104.03928831.224755717Hongshi/Jinshi39.47/5.736.76/0.64Low
Yinghua104.02788831.297691916Hongyang85.8769.08High
MianzhuJiulong104.13988931.411938969Hongshi/Jinshi44.00/3.878.69/0.43Low
Guangji104.11535031.257515617Hongshi/Jinshi38.13/2.278.19/0.25Low
Yuquan104.13212031.257500582Donghong/Huapu70.80/13.7314.61/1.53Low
Xiaode104.23935231.241509530Donghong77.2034.89Moderate
MianyangAnzhouHuangtu104.43596231.545840585Hongyang100.0093.76High
Sangzao104.33364931.593687661Hongyang100.0097.11High
BeichuanYongchang104.44037431.582567600Hongyang100.0087.05High
Guixi104.64789331.987493893Hongyang79.0749.20Moderate
Tongquan104.60875431.770263722Hongyang93.7383.45High
MeishanPengshanXiejia103.70615030.262840550Hongyang99.2094.06High
DongpoFuniu103.94280330.089608471Hongyang94.6759.27Moderate
Table 4. Pearson correlation analysis between the occurrence of kiwifruit brown spot and varieties and altitude.
Table 4. Pearson correlation analysis between the occurrence of kiwifruit brown spot and varieties and altitude.
Incidence RateDisease Index
Correlation CoefficientSignificanceCorrelation CoefficientSignificance
varieties0.929 **0.0020.795 *0.033
altitude−0.780 **0.000−0.604 **0.000
Note: * and ** indicate p < 0.05 and 0.01, respectively.
Table 5. The accumulated contribution of each environmental variable to the potential distribution of kiwifruit brown spot.
Table 5. The accumulated contribution of each environmental variable to the potential distribution of kiwifruit brown spot.
VariablesContribution (%)Cumulative (%)
bio325.825.8
tmin820.946.7
tmin617.063.7
prec816.780.4
tmax73.183.5
prec22.285.7
prec42.187.8
tavg101.589.3
bio21.490.7
tmin71.492.1
prec61.193.2
Table 6. Pearson correlation analysis of environmental variables affecting the distribution of kiwifruit brown spot.
Table 6. Pearson correlation analysis of environmental variables affecting the distribution of kiwifruit brown spot.
bio2bio3prec2prec4prec6prec8tavg10tmax7tmin6tmin7
bio30.924
prec2−0.370−0.154
prec4−0.475−0.5240.501
prec6−0.321−0.0310.7050.427
prec80.0800.2570.6640.1000.327
tavg10−0.613−0.5550.4150.2160.1010.288
tmax7−0.705−0.7670.2490.4270.0110.0080.897
tmin6−0.688−0.7300.2440.301−0.0860.1360.9420.958
tmin7−0.766−0.7970.2900.3980.0250.0740.9240.9830.983
tmin8−0.781−0.8060.2960.3980.0410.0770.9180.9770.9800.996
Table 7. Prediction of the potential distribution area of kiwifruit brown spot (regions).
Table 7. Prediction of the potential distribution area of kiwifruit brown spot (regions).
RegionUnsuitable AreaLowly Suitable AreaModerately Suitable AreaHighly Suitable Area
Area (km2)Proportion (%)Area (km2)Proportion (%)Area (km2)Proportion (%)Area (km2)Proportion (%)
Aba84,075.1626.42672.300.70205.430.41168.080.77
Bazhong1550.030.497152.557.473884.417.7318.680.09
Chengdu747.000.232931.993.064594.079.146144.1028.12
Dazhou3828.391.2012,381.5712.94448.200.890.000.00
Deyang336.150.112670.532.792241.014.46877.734.02
Ganzi149,157.7846.88373.500.39280.130.560.000.00
Guang’an653.630.215509.155.760.000.000.000.00
Guangyuan1848.830.584519.374.729412.2318.73597.602.74
Leshan1624.730.513735.013.904594.079.142801.2612.82
Liangshan55,203.5017.351998.232.09989.781.97859.053.93
Luzhou298.800.097376.657.713716.347.40392.181.79
Meishan448.200.141755.461.833678.997.321344.606.15
Mianyang5303.721.679057.419.465714.5711.37541.582.48
Nanchong0.000.0011,690.5912.211064.482.120.000.00
Neijiang0.000.004911.545.13466.880.930.000.00
Panzhihua7245.932.280.000.000.000.000.000.00
Suining0.000.005322.395.560.000.000.000.00
Ya’an5863.971.842334.382.442297.034.574575.3920.94
Yibin0.000.003959.114.145602.5211.153529.5916.15
Ziyang0.000.005733.255.990.000.000.000.00
Zigong0.000.003305.493.451064.482.120.000.00
Total318,185.83100.0095,709.73100.0050,254.61100.0021,849.83100.00
Table 8. Prediction of the potential distribution area of kiwifruit brown spot (central planting areas).
Table 8. Prediction of the potential distribution area of kiwifruit brown spot (central planting areas).
RegionCountry (District)Unsuitable AreaLowly Suitable AreaModerately Suitable AreaHighly Suitable Area
Area (km2)Proportion of Whole Area (%)Area (km2)Proportion of Whole Area (%)Area (km2)Proportion of Whole Area (%)Area (km2)Proportion of Whole Area (%)
ChengduDujiang186.7515.8753.954.7689.927.941132.9571.43
Pujiang0.000.000.000.000.000.00629.42100.00
Qionglai0.000.000.000.0089.926.671348.7593.33
DeyangMianzhu261.4520.59197.8216.18251.7720.591222.8742.65
Shifang130.7315.5653.956.67305.7237.78809.2540.00
Guangyuan Cangxi0.000.00107.904.621924.2282.31317.4813.08
Mianyang Anzhou56.034.5589.927.58773.2965.151186.9022.73
Ya’anLushan205.4317.1989.927.81305.7226.561150.9448.44
Mingshan0.000.000.000.000.000.00593.45100.00
Yucheng0.000.000.000.0071.936.781061.0293.22
Table 9. Detailed information of the actual survey points for the field test.
Table 9. Detailed information of the actual survey points for the field test.
RegionCountryTownLongitudeLatitudeAltitude (m)VarietiesIncidence Rate (%)Disease
Index
Occurrence LevelSuitability Level
ChengduDujiangyanTianma103.729050 31.032388 601 Hongyang10097.53HighHigh
103.743516 31.025524 600 Hongyang10097.69HighHigh
103.756496 31.020132 621 Hongyang10098.76HighHigh
Juyuan103.657528 30.949170 653 Hongyang10093.82HighHigh
PujiangFuxing103.443221 30.317316 538 Hongyang98.1390.77HighHigh
103.438191 30.321275 546 Hongyang98.890.18HighHigh
103.436934 30.325817 528 Hongyang97.8786.86HighHigh
Datang103.418606 30.299636 587 Hongyang94.9388.53HighHigh
Daxing103.397353 30.235533 569 Hongyang96.1390.03HighHigh
Qionglai Sangyuan103.469178 30.461789 517 Hongyang/Donghong93.60/73.0789.77/16.39HighHigh
Kongming103.466594 30.342379 607 Hongyang93.0788.73HighHigh
Guyi103.516878 30.373997 586 Hongyang93.8793.17HighHigh
Baolin103.517850 30.331534 604 Hongyang91.8795.97HighHigh
103.516878 30.373990 589 Hongyang94.889.44HighHigh
ChongzhouQiquan103.641074 30.563695 438 Hongyang/Donghong100/77.4798.36/31.73HighHigh
103.660735 30.560634 451 Hongyang/Donghong100/85.6097.60/27.76HighHigh
Ya’anYuchengShangli103.059266 30.152868 963 A. arguta12.131.26LowHigh
103.070186 30.159260 968 Gold 35.730.64LowHigh
Duoying102.914164 30.015172 587 Hongyang89.8793.64HighHigh
BaoxingMuping102.832564 30.408815 1104 Hongyang82.870.53HighHigh
YingjingQinglong102.877242 29.767267 1091 Hongyang/Chuanmi 84.87/37.8674.49/25.21HighHigh
ShimianAnshunchang102.258098 29.310755 1399 Hongyang82.9372.55HighHigh
GuangyuanCangxiTingzi105.859244 31.819290 449 Hongyang93.674.4HighHigh
Yunfeng106.004130 31.715040 490 Hongyang90.472.09HighHigh
106.002725 31.724609 580 Hongyang87.8768.98HighHigh
106.018840 31.879743 519 Hongyang/Jinhong88.80/32.4066.85/15.45HighHigh
Lingjiang105.977369 31.799844 696 Hongyang84.1361.05ModerateModerate
Yongning106.002692 31.724439 588 Hongyang81.0764.03ModerateModerate
105.916557 32.002183 699 Hongyang78.5359.82ModerateModerate
Longwang105.959645 31.981199 681 Hongyang79.8762.39ModerateModerate
JiangePuan105.449204 32.127941 704 Hongyang74.1354.56ModerateModerate
105.422221 32.008581 686 Hongyang77.4756.12ModerateModerate
Longyuan105.450482 31.986242 671 Hongyang72.852.83ModerateModerate
QingchuanZhuyuan105.355354 32.249336 567 Hongyang76.1345.14ModerateModerate
DeyangMianzhuGuangji104.069418 31.260198 661 Hongyang94.481.97HighHigh
Jiulong104.126292 31.380313 701 Hongyang91.7376.93HighHigh
104.124498 31.390861 716 Gold 32.930.33LowHigh
MianyangAnzhouHuangtu104.435304 31.545761 578 Hongyang10097.09HighHigh
104.425117 31.569665 627 Hongyang10098.27HighHigh
104.440072 31.551297 635 Hongyang10093.66HighHigh
LeshanMabianLaodong103.562148 28.946852 1023 Jinhong16.41.82LowHigh
103.575287 28.938294 1022 Gold 37.870.87LowHigh
LuzhouXuyongHuangni105.348891 28.004857 1006 Gold 311.61.29LowHigh
GulinDongxing106.090053 27.984000 1180 Guichang13.731.52LowModerate
Yonghe105.915008 28.067051 463 16.531.84LowLow
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Zhu, Y.; Yao, K.; Ma, M.; Cui, Y.; Xu, J.; Chen, W.; Yang, R.; Wu, C.; Gong, G. Occurrence Regionalization of Kiwifruit Brown Spot in Sichuan. J. Fungi 2023, 9, 899. https://doi.org/10.3390/jof9090899

AMA Style

Zhu Y, Yao K, Ma M, Cui Y, Xu J, Chen W, Yang R, Wu C, Gong G. Occurrence Regionalization of Kiwifruit Brown Spot in Sichuan. Journal of Fungi. 2023; 9(9):899. https://doi.org/10.3390/jof9090899

Chicago/Turabian Style

Zhu, Yuhang, Kaikai Yao, Miaomiao Ma, Yongliang Cui, Jing Xu, Wen Chen, Rui Yang, Cuiping Wu, and Guoshu Gong. 2023. "Occurrence Regionalization of Kiwifruit Brown Spot in Sichuan" Journal of Fungi 9, no. 9: 899. https://doi.org/10.3390/jof9090899

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