Monitoring of Wheat Scab Using the Specific Spectral Index from ASD Hyperspectral Dataset

It is highly important to accurately monitor wheat scab and provide technical guidance for the crop pests and diseases. In this study, relevant analysis was performed among spectral reﬂectance, ﬁrst-derivate data, and the disease severity data through ASD hyperspectral data. Two sensitive spectral wavelength ranges of 450–488nm and 500–540nm were selected. Then, a new wheat scab index (WSI) consisting of the two bands was proposed. The inversion models of the scab severities were comparatively built by unitary linear regression and multiple stepwise regression techniques. The results showed that the WSI had a signiﬁcant linear relationship with severity of disease compared with other commonly used spectral indices. The ﬁtting R 2 , testing R 2 , and RMSE were 0.73, 0.70, and 13.41, respectively. The multiple stepwise regression model established using the WSI, SD g /SD b , NBNDVI, and SD g as independent variables was better than the single-variable model. Our results suggest that WSI can be used to provide scientiﬁc guidance for monitoring and precise management of wheat scab disease.


Introduction
China is a big agricultural country with vast land and abundant agricultural resources. Wheat is the second largest food crop in China, and its planting area ranks second. During the growth period of wheat, the occurrence of some pests and diseases will seriously affect the yield and quality. As one of the seriously infected diseases, wheat scab caused by a variety of Fusarium is a widespread and global disease occurring in warm and high-humidity environments [1]. According to the statistics, when the severe occurrence of wheat scab disease is about 50%∼100%, the yield can be reduced by 40% [2]. Conventional stress-detection methods depend on physiological and biochemical analysis by field pathologists or experienced people. ey are usually destructive, time-consuming, and labor-intensive. It is difficult to adapt to the current urgent needs of large-scale, real-time monitoring, and forecasting of pests and diseases [3,4]. erefore, how to quickly and accurately monitor wheat scab is an urgent problem to be solved.
Studies have shown that [5] some spectral characteristics change when vegetation is stressed. For example, the red edge will move to the shortwave direction when a plant is suffering from stress, and it is called "blue shift." is phenomenon usually takes place with the displacements of only a few nanometers to twenty nanometers [6]. It is difficult to capture this displacement using the traditional wide-band remote sensing data with hundreds of nanometers wide. Conversely, hyperspectral data with abundant band information and high resolution were used to detect the spectral response to diseases in more studies [7]. Many scholars used the hyperspectral data to analyze the spectral reflectance and found the sensitive bands for disease identification. For example, Graeff et al. [8] pointed out that the six wavebands of 490 nm, 510 nm, 516 nm, 540 nm, 780 nm, and 1300 nm could produce significant spectral responses to wheat powdery mildew. Huang [9] proposed that the spectral regions of 630-687 nm, 740-890 nm, and 976-1350 nm were sensitive to stripe rust. Delwiche and Kim [10] found that wheat scab could cause spectral responses at 550 nm, 568 nm, 605 nm, 623 nm, 660 nm, 697 nm, 715 nm, and 733 nm. Different plants have different spectral characteristics, but the same plant may have different spectral characteristics at different growth stages and environments [7]. e response of the spectra to changes in plant physiology, biochemistry, morphology, and structure is highly complex. It is sometimes difficult to reflect the corresponding information accurately only through the initial spectral reflectance. Some more specific spectral indices can be proposed based on the hyperspectral data. e spectral index can realize the identification and monitoring of different diseases by filtering and combining original bands. Bravo et al. [11] used the normalized difference vegetation index (NDVI) to extract the wheat stripe rust using discriminant analysis with an overall accuracy of over 95%. Zheng et al. [12] proved that the three-band spectral indices PRI (570, 525, and 705 nm) and ARI (860, 790, and 750 nm) are optimal for monitoring yellow rust infection at different growth stages. Jiang et al. [13] found that the ratio of the first-order differential sum (SD r ′ ) in the red region (725-735 nm) to the first-order differential sum (SD g ′ ) in the green region (520-530 nm) is sensitive to the early symptoms of wheat disease. e correlation coefficient with the disease index reaches 0.921, indicating the differential vegetation index SD r ′ /SD g ′ is suitable for early diagnosis of wheat diseases.
Although many studies have been conducted on wheat disease, there is little research on scab. Most of the scholars used hyperspectral data to study stripe rust, powdery mildew, and aphid on leaf or canopy scale. Scab is a typical ear disease, so a proprietary index that can be used to monitor wheat ear-scale scab is desirable. erefore, based on previous studies, our study aimed (1) to identify wavebands that are sensitive to wheat scab at ear scale; (2) to construct a new spectral index (WSI) for characterizing the spectral changes caused by scab infestation; and (3) to evaluate the performance of the proposed WSI for retrieving scab severities using linear regression method.

Study Site.
e experiment was carried out at a test field in Guohe Town, Lujiang County, Anhui Province (31°25.6′N, 117°9.2′E), on May 8, 2018 ( Figure 1). Rich water resources and suitable climate provide favorable conditions for the incidence of wheat scab, so the disease occurs almost every year. e wheat cultivars "Yangmai," "Ningmai," and "Wanxi" were selected as the experimental samples because of their moderate susceptibility to scab. e sowing time of wheat was around October 2017, and the harvesting time was around mid-June 2018. e test time was in GS stages when the scab showed severe infection.

Spectral Acquisition of Wheat Ear.
e spectral reflectance of the wheat ear was collected with an ASD FieldSpec Pro spectrometer (350-2500 nm) with the spectral resolution of 3 nm during the 350-1000 nm and 10 nm within the 1000-2500 nm range. Measurements were taken at sunny noon time (10 : 00-14 : 00). During the measurement, every wheat ear was placed in the middle of the black cloth, and the probe of the sensor was held vertically downward to measure the upright, front, and side data. A 40 cm × 40 cm BaSO 4 calibration panel was measured to correct the reflectance. e spectra in different directions for each sample were measured 20 times, and then the mean was used as the reflectance. Hyperspectral data for the front, side, and upright sides of each wheat ear were finally determined. e calculation formula is as follows: where R 1 is the target reflectance, DN 1 is the gray value of the target spectrum, DN 2 is the gray value of panel, and R 2 is the panel reflectance.
In the experimental field, 41 sample plots were selected and an infected wheat was randomly selected as our research sample from each sample plot. A total of 41 infected wheat samples were obtained with different severity levels from the field survey ( Figure 2). Each sample data was averaged from the front, side, and upright spectral reflectance. e healthy samples were not collected in this survey. According to the calculation of disease severity, the samples of levels 1-4 were 10, 13, 12, and 6, respectively. e spectral curve of wheat ears had serious noises after 1330 nm, so the 350-1330 nm was selected in this study.

Calculation of Spectral Differential.
In order to analyze the spectral response characteristics of wheat scab, we averaged the sample spectral reflectance of each level. A correlation analysis was performed between spectral reflectance and disease severity was used to pick up the sensitive positions and ranges. However, due to the influence of noise, we failed to achieve good results through the original spectral reflectance. e spectral differential was used to reduce external influences, and its formula is as follows [14]: where λ i is the wavelength of the band i, P′(λ i ) is the differential value of λ i , P(λ i + 1) and P(λ i − 1) are the previous and next spectral reflectance of λ i , respectively, and Δλ is the difference of λ i− 1 to λ.

Leave-One-Out Cross Validation.
Leave-one-out cross validation was applied to verify the classi cation accuracy. Its main idea [12] is that one sample is rst selected randomly from the N samples, and the other N− 1 samples are used as the training samples. A model will be obtained to verify the accuracy with the selected single data, so repeat N times. e root mean square error (RMSE) was used to evaluate the model shown as follows [14]: where y i and y ∧ i represent the measured value and the predicted value, respectively, and n is the total number of samples. e smaller the RMSE is, the higher the prediction accuracy of the model is.

Selection of Vegetation Index and Di erential Spectral
Characteristics. Spectral indices are widely used for monitoring, analyzing, and mapping temporal and spatial variation in vegetation [15]. Spectral indices are the basis for wide applications in remote sensing-based crop management because they are highly correlated to biophysical and biochemical crop variables [16]. Infected crops can cause changes in pigment, water, morphology, structure, etc. Some indices can characterize these changes, for example, NDVI can re ect the growth of crops and NRI (nitrogen re ectance index) is a factor to study the nitrogen content of vegetation. We summarized the spectral features commonly used in crop stress through the literature review. A total of 22 spectral features including rst-order differential spectral features and vegetation indices were selected (Table 1).

Unitary Linear Regression.
e unitary linear regression is a relationship between an independent variable and a dependent variable. It is the simplest regression Th e Y a n g t z e R i v e r where y is the dependent variable, x is the independent variable, and a and b are the regression constants.

Multiple Stepwise Regression.
Multiple stepwise regression algorithm is often used for regression analysis of two or more independent variables and dependent variables. e main principle is to determine its importance by the Ftest for each introduced variable. Meanwhile, the T-test is performed on the variables introduced into the model. When the first introduced variable is no longer significant for the dependent variable due to the introduction of new variables, the variable will be deleted. Only the important variable is retained in the regression model. Assuming there are n independent variables (x 1 , x 2 , . . . , x n ) and y is used as the dependent variable, then the multiple stepwise regression model is defined as follows [31]: y � a 1 x 1 + a 2 x 2 + · · · + a n x n + a 0 , where a i (i � 0, 1, . . . , n) is the pending regression constant.

Spectral Response Characteristics and Correlation
Analysis. It can be seen from Figure 3 that with increasing disease levels, the spectral reflectance of scab-infected wheat decreases in the near-infrared region, while it increases in the visible region and the "green peak" and "red valley" gradually become gentle. is is because when the crop is infected by pathogens, it will cause many lesions, necrosis, or wilting in the leaves of the plants. e content and activity of the pigments are reduced, resulting in an increase in the reflectance of the visible region. Moreover, the water metabolism of infected plants will be disturbed, which will cause the water deficit of the leaves to some extent, and finally cause the change of reflectance in the near-infrared region [32].
It can be seen that the visible region is positively correlated with the severity of scab, and the near-infrared region is negatively correlated with the severity of scab (Figure 4). e band with a correlation coefficient greater than 0.5 in the visible region (350-740 nm) is 638-690 nm, and the 674 nm has a highest correlation coefficient (R � 0.598), which is located in the red region. Because the photosynthesis ability of wheat is weakened due to the influence of scab, the correlation coefficient of chlorophyll absorption zone is increased. In addition, the correlation between the nearinfrared region (760-1300 nm) and the disease severity is generally low. e reason may be that the internal structure of the cell is destroyed and the reflectance is reduced. e spectral reflectance of 764 nm in the near-infrared region has a highest negative correlation (R � − 0.411). According to the aforementioned analysis, wheat scab has a response in the visible and near-infrared region. It showed a strong response Maximum first-order differential value of the blue edge (490-530 nm) [28] D y Maximum first-order differential value of the yellow edge (550-582 nm) D r Maximum first-order differential value of the red edge (670-737 nm) SD b e sum of first-order differential value of the blue edge SD y e sum of first-order differential value of the yellow edge SD r e sum of first-order differential value of the red edge SD g e sum of first-order differential value of the green peak (510-560 nm) [29] SD g /SD b e ratio of SD g to SD b SD y /SD b e ratio of SD y to SD b (SD r − SD y )/(SD r + SD y ) Normalized ratio of SD r and SD y (SD g − SD b )/(SD g + SD b ) Normalized ratio of SD g and SD b 4 Journal of Spectroscopy in the visible region wavebands, but the correlation between the original spectral data and the severities of scab was not high.

Extraction of Sensitive Bands Based on Spectral Differentiation and Correlation Analysis.
According to the firstorder differential spectral curve of four disease severities ( Figure 5), they are different in the visible region of 450-740 nm. As the disease level increases, we can see the differential values of 500-550 nm and 690-720 nm are gradually decreasing, as well as increasing in the region of 550-610 nm. e regions of 500-550 nm and 550-610 nm are located on both the sides of the "green peak", indicating that the spectral reflectance curve become gentler in the two regions, which is consistent with the observation of the above spectral reflectance. Correlation analysis was used to assess whether significant relationships existed between the first-order differential and the wheat scab disease levels ( Figure 6). It could be found that 601 nm had the highest correlation (R � 0.79), which was located near the right side of the "green peak." All the correlation coefficients of 450-488 nm, 500-540 nm, 552-667 nm, and 687-756 nm were greater than 0.5. e correlation between the first-order differential and the scab severity is better than that between the spectral reflectance and disease severity.

Construction of Wheat Scab
Index. According to the above analysis, the correlation between the original spectral data and the disease is not significant, while the first-order spectral differential has a good correlation with wheat scab.
ere are four significant correlations between first-order differential and disease severity during the 450-488, 500-540, 552-667, and 687-756 nm. e four wavelength ranges  are located in the chlorophyll absorption zone, the blue edge, the yellow edge, and the red edge, respectively. When vegetation is infected by disease, the spectral reflectance of the chlorophyll absorption zone changes with the chlorophyll content. Relevant studies have shown [33] that the blue, yellow, and red edge of plants can be used to monitor crop pests and diseases. erefore, this section attempts to use the first-order spectral differential sum of these four bands to construct the scab index. As these four wavebands are adjacent to each other, the sum of the first-order differential values of the four bands may have redundancy. erefore, we make correlation analysis of the first-order differential sum of the four band intervals and choose the weakly correlated bands of 450-488 nm and 500-540 nm to construct the wheat scab index (WSI). e correlation coefficient between different wavebands and the method to construct WSI are shown in Table 2 and formula (6), respectively.

Unitary Linear
Regression. e purpose of this experiment is to analyze the sensitivity of existing vegetation indices and spectral differential characteristics to wheat scab under linear regression conditions and to verify the applicability of the proposed scab index. Table 3 summarizes the unitary linear regression responses of all spectral indices (including WSI) to wheat scab disease. We found that the selected 23 indices manifested excellent potential for discriminating wheat scab (p < 0.001). However, not all the       Journal of Spectroscopy selected spectral indices were able to significantly discriminate wheat scab. Specifically, WSI showed the highest fitting R 2 of 0.73, followed by NBNDVI, NDVI, and SD y with fitting R 2 of 0.67, 0.66, and 0.64, respectively. It can be found that most fitting R 2 are not high. Leave-one-out cross validation was used for the accuracy verification for the regression results of all indices (Table 3). e results prove that WSI has the highest accuracy (testing R 2 � 0.70; RMSE � 13.41), which indicates it can perform well in identifying wheat scab of different levels on the ear scale.

Multiple
Stepwise Regression. Related studies have shown that the model established by multiple variables is better than that by single variable [34]. e multiple stepwise regression statistical method was used to calculate the relationship between spectral indices and disease severities. Taking all the 23 spectral indices as independent variables and the disease severity as the dependent variable, it can be known that the final variables of the model are WSI, SD g / SD b , NBNDVI, and SD g (Table 4). en, the multivariate stepwise regression equation is obtained as follows: − 984.01SD g + 276.882.
e multiple regression model was compared with three unitary regression models with high fitting R 2 (Figure 7). We find that the multiple regression model produced the highest fitting R 2 of 0.79 and more even distribution. To further validate the ability of the model constructed by WSI, SD g / SD b , NBNDVI, and SD g to detect wheat scab disease, we used leave-one-out cross validation; scatter plots of the relationship between the actual severity and predicted severity are shown in Figure 8. e multiple stepwise regression showed a testing R 2 of 0.72 and an RMSE of 13.02, respectively, indicating that the integrated model based on WSI, SD g /SD b , NBNDVI, and SD g has a better inversion effect on the severity of disease than the single variable.

Conclusions
e timely monitoring of wheat scab disease is critical for agricultural management. By analyzing the correlation between first-derivate spectra and corresponding disease severity levels, two sensitive wavebands (450-488 nm and 500-540 nm) were selected. Subsequently, a new index (WSI) was developed for detecting and monitoring wheat scab at the ear scale. Compared with other common spectral indices, WSI has excellent performance with the fitting R 2 of 0.73, testing R 2 of 0.70, and RMSE of 13.01, respectively. Moreover, the multiple regression model is more conducive to the identification of scab than univariate regression models. Our study can provide the technical support for the early diagnosis and management of wheat scab.

Data Availability
e data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest
e authors declare that they have no conflicts of interest.   Journal of Spectroscopy