ABSTRACT

1. Introduction
Many plants show symptoms of necrosis at the leaf tip and margin when they are affected by extreme environmental conditions such as s lt toxicity, water stress, high/low temperature, nutrition deficiency, injured root and trunk, transplanting shock, and dis- ease (Treshow, 1970; Durbin, 1978). Typhoons are one kind of disaster that can cause serious mechanical damage to trees and shrubs, for example, by uproot- ing, stem breaking, bending and leaning, and so o n (Takahashi et al., 1981; Yamamoto, 1979; Nobel, 1981; Maki et al. , 1991). They are also complex ca- lamities that can induce many unfavorable extreme conditions like flooding, gusty winds, and drought as well as salt/sand spray, which cause plants physiologi- cal injury (Maki et al., 1991; Nobel, 1981). Ginkgo (Ginkgo biloba L.) is a showy landscape tree species, which is widely planted in China, Japan, and so o n. However, it often shows leaf necrosis (Okinaka et al., 1990) and branch dieback (Shimizu, 2004) after dam- age by high temperature (Treshow, 1970) or by strong dry typhoon, especially along the coast. Typhoon 0613 was characterized by low pre- cipitation and high wind speed with maximum gusty wind speed of 42.4 m/s, maximum wind speed of 20 m/s, and precipitation of 26 mm when it hit Yamagu- chi City. However, during the hit, as the maximum wind speed reached its peak value, there was almost no rainfall. This  rainless or less-rain period persisted more than one month after the hit. Following Typhoon 0613, it is observed that leaf necrotic symptoms ap- peared on many landscape trees and shrubs in Yama- guchi City, particularly ginkgo. It made the crowns of ginkgo trees obviously different between the windward and leeward sides, which became a prob- lem to be studied in this paper. This kind of damage has also been reported in other papers. Ginkgo trees with symptoms of leaf necrosis extended inland even as far as 100 km from the coastline during the hit by Typhoon 8218 in the area of the Kanto plain, Japan (Okinaka et al., 1984). However, the visual scale method was more common in research on ginkgo crowns damaged by typhoons. In this paper, spectral reflectance was used to estimate the damage status in order to find an objective method of estimation and evaluation. As an important non-destructive approach, the near-infrared spectral analysis method has been wide- ly utilized in the area of agriculture and medicine and the food, fiber, and chemistry industries. In the field of agriculture, it was originally used for the things with lower water content, and its application in fruits, vegetables, and crops with higher water content began in modern times (Iwamoto et al., 1994). However, spectral reflectance measurement has been used to estimate the plant leaf area index (Yamamoto, 1998), chlorophyll concentration (Carter et al., 1994, 2001; Ito et al., 2003), nutrient elements (Hinzman et al., 1986), water content (Yamamoto et al., 1995; Carter et al., 1993; Ito et al., 2003), and so on. Carter et al. (1994) considered that spectral reflectance in narrow wavebands within the 690- to 700-nm range and its ratio to near-infrared reflectance should provide ear- lier detection of stress-induced chlorosis compared with broad-band systems or narrow bands located at lesser wavelengths. Ito et al. (2003) diagnosed the chlorophyll content by the ratio of spectral reflectance at 800 nm and 680 nm. Under water stress, and the change of plant spectral reflectance in the near-infra- red range has been reported in some other researches (Holben et al., 1983; Jackson et al. 1985; Moran et al., 1989; Yamamoto et al., 1995; Penuelas et al., 1999). Thorhaug et al. (2006) stated that browning and necrosis resulted in a clear change in the shape of the reflectance spectra of Thalassia blades and sug- gested that the reflectance spectra at 750 nm might be a suitable stress index. Riedell et al. (1995) noted that crop canopy chlorosis and necrosis in small grain fields infested with greenbugs, etc. could be used as a diagnostic tool to detect crop damage from cereal aphid population outbreaks. Yamamoto et al. (1996) reported that it was possible to detect the leaf area of soybean damaged by the common cutworm with the normalized difference vegetation index (NDVI) at 750/600 nm. Steddom et al. (2005) reached the con- clusion that the use of radiometric methods has the potential to increase the precision of assessment of Cercospora leaf spot foliar symptoms of sugar beet while eliminating potential bias. Nevertheless, whether or not it can be used in estimating the damage status of landscape trees hit by strong typhoons like Typhoon 0613 still needs to be researched. What is the optimum wavelength for evaluating the damage status and are there any differ- ences among tree species and trees planted at different sites of different distances from the coastline? In this study, after selecting the optimum spectral reflectance wavelength, leaf necrosis of ginkgo trees induced by Typhoon 0613 was estimated by spectral reflectance analysis combined with the visual scale method. By measuring the necrotic area percentage (NAP) and NDVI of necrotic leaves, the relation between them and the difference in the spectral reflectance of gink- go leaves among different sites and between ginkgo and other tree species were studied.
2. Materials and Methods
In this research, three experiments were carried out. The first was to study the percentage of differ- ently necrotic leaves in the crowns of ginkgo trees. The second was to study the difference in spectral re- flectance between ginkgo and other tree species after being hit by Typhoon 0613. The third was to study the difference in ginkgo leaf necrosis among three sites of different distances from the coastline.
2.1 Measurement of leaf necrotic percentage
and spectral reflectance
To study the percentage of necrotic leaves in the crowns of ginkgo trees, six standard branches, three from the leeward side and three from the windward side, from three trees in a shelterbelt were sampled from Yamaguchi University. All the leaves on the branches were visually divided into five necrotic lev- els according to the necrotic area percentage. After counting the leaf number, the spectral reflectance for leaves of each level was measured respectively by a radiometer, EKO-MS720, made by EKO Instruments Co. Ltd. Its spectral resolution is 10 nm, its interval of wavelength is 3.3 nm, and the spec- ified wavelength ranges from 350 to 1050 nm. Leaves were measured with a special method in an indoor en- vironment in order to avoid the effect of the gap frac- tion (Ito et al., 1996) and light condition between the windward and leeward sides of trees in the field mea- surement, because it is not easy to obtain comparable spectral reflectance data for trees under these condi- tions. The radiometer was mounted on a tripod 30 cm above the sample leaves. A tray of 20×30×4 cm and vertically measured under a 40-w incandescent lamp was smoothly filled with the sample leaves. A field of view of 25° was selected and the area coverage was 139 cm², approximately equal to a circular area with a diameter of 14 cm. Measurements were controlled by a piece of white paper corrected by a standard white board of barium chloride, and three duplications for each level were conducted at different positions on the tray. The spectral reflectance was used to calculate the NDVI by Equation (1):
where NIRm is the spectral reflectance in the near-infrared region, VIBn is the spectral reflectance in the visible region, m = 750, 760, ………, 900, and n = 630, 640,………, 690. According to the wavelength analysis, the optimum wavelength for calculating the NDVI was 755 nm and 679 nm for NIR and VIB. Therefore, all NDVI values and NDVI using ratio (NDVIr) values in the paper were calculated by the spectral reflectance value at these two wavelengths except the NDVI value in the optimum wavelength analysis.
2.2 Measurement of NAP
The leaves were scanned with a Canon D125u2 scanner, and the NAP of each leaf was calculated by the image pixel method. NAP is the proportion of ne- crotic area to overall leaf area. It was determined by obtaining pixels of the overall leaf and then separat- ing the green part (refer to Fig. 1) from the leaf with the eraser tool of Photoshop. The NAP was calculated by Equation (2), and the NAP value for the level of each leaf was the average NAP value of every leaf on the related scale. (2)
2.3 Measurement for comparison between
ginkgo and other tree species
The tree species used for comparison with gink- go include metasequoia (Metasequoia glyptostrobo- ides Hu et Cheng), trident maple ( Acer Buergerianum Miq.), and kaizuka juniper ( Sabina chinensibs L.), which are widely planted in Yamaguchi City. Leaves were mechanically sampled from shelterbelts of ginkgo, metasequoia, and kaizuka juniper, and from an individual trident maple tree in Yamaguchi Uni- versity. The spectral reflectance for leaves of every species was measured by the method mentioned in 2.1 with four duplications for each species. The average of the four duplications of spectral reflectance was used to calculate the NDVI value by Equation (1). The NDVIr is an average value between the NDVI value for leaves on the windward side and the NDVI value for leaves on the leeward side. It was calculated NDVI for leaves on windward + NDVI for leaves on leeward NDVIR = 2.4 Measurement for comparison among three sites To study the difference in leaf necrosis among sites of different distances from the coastline, Site A, Site B, and Site C were selected. Site A is located at Tokusa in Anno Canyon, Site B, at Yamaguchi besides the Fusino River, and Site C, at Ube near Yamaguchi Bay, which are 40.1, 12.6, and 1.7 km away from the coastline, respectively. Sampling and measurement were carried out on Nov. 1 and Nov. 2, 2006 for Site A and Site B and on Nov. 6 and Nov. 8, 2006 for Site C. The distance from the coastline (DC) is the short- est distance from any of the three sites to the coastline measured by an electronic atlas tool named Atlas Z Proffessional5. Meteorological data for these three sites were obtained from the Automated Meteorologi- cal Data Acquisition System of Japan. Six standard branches, three from the wind- ward side and three from the leeward side, were also sampled for each of the three sites, respectively. The method of leaf counting was the same as the above- mentioned scale method. The spectral reflectance for leaves of every site was also measured by the method mentioned in 2.1 with three duplications for each site. The average of the three duplications of spectral reflectance was used to calculate the NDVI value by Equation (1). The NDVIr values were also calculated by Equation (3).
3. Results and discussion
3.1 Selection of the optimal spectra wavelength
for the measurement of ginkgo leaves
After summarizing a number of studies con- cerned with responses to physiological stress, Carter et al. (2001) considered the maximum difference in reflectance within a 400- to 850-nm wavelength range between control and stressed states occurring at wave- lengths near 700 nm. Spectral reflectance is affected by strong chlorophyll absorption in the range of 670– 680 nm and changes with variation in leaf anatomy or water content in response to stresses beyond 730 nm in the near-infrared region (Carter et al., 2001). Slaton et al. (2001) considered that leaf reflectance in the near-infrared region is primarily affected by leaf structure and the position of the red edge correlated with chlorophyll content, plant phenological stage, as well as plant stresses. Leaf necrosis is characterized by chlorophyll loss and leaf drying as well as leaf structure variation. The optimal wavelength should exist in these regions. According to the definition of NDVI, many NDVI values can be calculated by measuring spectral reflectance. In this research, the proper wavelength for calculation of NDVI was determined by maxi- mum variance of NDVI for ginkgo leaves of different necrotic levels. Ginkgo leaves for selecting the opti- mal spectra wavelength were sampled from a ginkgo shelterbelt in Yamaguchi University. After measuring the spectral reflectance in the visible region and near- infrared region, the NDVI values for all of the wave- lengths from 600 to 900 nm were calculated. For the visible region, all the NDVI values were calculated by every spectral reflectance value in the visible re- gion and one definite spectral reflectance value from the near-infrared region at a wavelength of 755 nm (refer to Fig. 2-a). For the near-infrared region, all the NDVI values were calculated by every spectral reflectance value from the near-infrared region and one definite spectral reflectance value in the visible region at a wavelength of 679 nm, comparatively (re- fer to Fig. 2-b). From Figure 2-a and Figure 2-b, it is evident that the maximum variance of NDVI values is at wavelength 755 and 679 nm, respectively, and the same values are maintained when they are calculated by different definite spectral reflectance values.
3.2 Difference in leaf necrosis between the
windward and leeward sides of ginkgo trees It was observed that some landscape trees showed necrosis from the leaf tip and margin to the entire leaf after Typhoon 0613 hit, in which a large variance in necrosis of ginkgo leaves and a significant difference between the windward and leeward sides after Typhoon 0613 hit were observed (refer to Fig. 3). From Figure 3, it can be seen that most leaves lee- ward of the sampled crowns are non-necrotic leaves, overall green leaves account for 70.9%, and no leaves have become entirely brown. Most leaves windward of the sampled crowns are necrotic leaves and dried leaves, and only 7.83% of them were green overall. This means that it was the difference in the percent- age of necrotic leaves between the windward and leeward sides that made the crowns of the damaged ginkgo trees show different colors on either side of the crown. Many previous researches on typhoon dam- age to trees have involved ginkgo (Okinaka et al., 1984, 1990; Shimizu, 2004). However, researches on ginkgo seldom focus on spectral reflectance charac- teristics. The visual scale method has been more com- monly used to observe the damage characteristics of crowns (Okinaka et al. , 1984, 1990; Shimizu, 2004; Muhammed et al. , 2003), and few of them have been involved in the quantitative study of leaf necrotic area percentage. In this study, the results of spectral reflec- tance for different necrotic levels of ginkgo leaves showed a great difference, indicating an inverse liner relationship between NAP and NDVI 755nm/679nm , where R²=0.985 as shown in Figure 4. It means that the NDVI value decreases as the leaf necrotic area in- creases. The NDVI values corresponded well with the ginkgo leaf necrotic area. Evidently, it is possible to estimate the necrotic area by measuring the spectral reflectance of leaves.
3.3 Spectral reflectance of necrotic leaves of
different tree species
As mentioned above, many plants can show symptoms of leaf necrosis by damage due to extreme environmental conditions (Treshow, 1970). Spectral reflectance may be adopted to evaluate the necrotic status of other tree species besides ginkgo. By spec- tral reflectance analysis of leaves sampled from the windward and leeward sides of tree crowns after be- ing hit by Typhoon 0613, the kaizuka juniper, an ever- green typhoon damage-resistant tree species (Shimizu, 2004), obviously differed from the other three decidu- ous tree species. Almost no difference between the windward and leeward sides of the crowns of kaizuka juniper was found in the spectral reflectance curves since there was no necrosis of their leaves. For the other three deciduous tree species, the spectral reflec- tance curves between the windward and leeward sides can be clearly distinguished because there are more necrotic leaves on the windward side (refer to Fig. 5). From Table 1, a very clear difference between the evergreen kaizuka juniper and the other three deciduous tree species can be seen from NDVIr. The NDVIr of the crown is 43.9, 47.3, 43.6, and 75.1, respectively, for the sampled trees of ginkgo, metase- quoia, trident maple, and kaizuka juniper. The differ- ence among ginkgo, metasequoia, and trident maple was clearly smaller than the difference between the three deciduous trees and the kaizuka juniper. The reason seems to be the necrotic leaves on the wind- ward side of these deciduous trees and the different spectral reflectance sensitivity to them.
leeward side. 3.4 Difference in leaf necrosis among different sites According to this study, the spectral reflectance of leaf samples from sites with different DC also var- ied significantly. Figure 6 shows that almost all leaves sampled from ginkgo trees at Site A, which is more than 40 km from the coastline, were mainly non- necrotic leaves. By contrast, most leaf samples from Site C, less than 2 km from the coastline, were necrot- ic leaves and dried leaves. The leaf samples from Site B, about 13 km from the coastline, were in the middle position. Therefore, the difference in storm-damaged ginkgo leaves among sites was mainly due to the difference in the percentage of leaves with varying levels of necrosis after Typhoon 0613. The nearer to the coastline, the more leaves there are with serious necrosis after being hit by a typhoon. Figure 7 shows the spectral reflectance curves of ginkgo leaves sampled from three sites after being hit by Typhoon 0613. It is clear that there was also a big difference in spectral reflectance among the leaves sampled from the windward and leeward sides of ginkgo trees from the three sites. For the samples from Site A, with an NDVI value of 0.679 for both the leeward and the windward side, respectively, the spec- tral reflectance curves almost overlapped each other so that they could not be distinguished from each other. This means almost no difference in leaf spectral 7 reflectance between the windward and leeward sides of ginkgo trees at this site. Although the samples from Site B and Site C showed a similar tendency whereby the spectral reflectance curves between the windward and leeward sides of the ginkgo trees were separate from each other, we can clearly find a difference. The spectral reflectance for the leaves of ginkgo trees at Site B, with an NDVI value of 0.749 and 0.373 for the leeward and the windward side, respectively, was significantly higher than that of Site C with an NDVI value of 0.528 and 0.096 for the leeward and wind- ward sides. This implies that Site C contained more necrotic leaves. It is evident that the spectral reflec- tance characteristics are consistent with the result of the visual scale observation. Compared to the NDVI value, the NDVIr value corresponded better to the damage status of ginkgo trees, which combined the spectral reflectance of both the windward and leeward sides. Figure 8 shows the NDVIr, DC, maximum wind speed, and precipitation during Typhoon 0613 for the three sites. The NDVIr values were respectively 67.9, 56.1, and 31.2 for Site A, Site B, and Site C. The related maximum wind speeds were respectively 8, 20, and 27 m/s, rainfall, 52, 26, and 14 mm, and distance from coastline, 40.1, 12.6, and 1.7 km.  This means that the nearer to the coastline, as the wind speed increased accompanying the decrease in rainfall during Typhoon 0613 for the investigated sites, the smaller the NDVIr values were. In other words, the nearer to the coastline, the greater the leaf necrosis of ginkgo. The result of spectral re- flectance was well in accordance with the difference in wind and precipitation. It was also consistent with the result of the visual scale observations of other re- searchers (Okinaka et al., 1984).
4. Conclusion
Based on this research, it is the difference in leaf necrotic status between the windward and leeward sides of ginkgo crowns that causes the variance in dis- coloration between them. This kind of variation also appears at sites of different distances from the coast- line. They can be estimated by measuring the spectral reflectance of ginkgo leaves with different necrotic status by using the pocket radiometer, EKO-MS720. The optimum wavelength for the calculation of NDVI for necrotic ginkgo leaves is 679 and 755 nm. The result of measurement of NDVI 755nm is very con- sistent with the result of direct visual observation, and the close inverse relationship between NDVI 755nm/679nm and NAP of ginkgo leaves indicates that it has poten- tial to evaluate the damage status of ginkgo and to be an alternative tool to measure leaf necrosis induced by typhoons like Typhoon 0613, especially by using the NDVIr value. Comparison between ginkgo and three other tree species indicated that spectral reflectance was more sensitive for the three deciduous tree species with necrotic leaves than for the evergreen kaizuka juniper tree without necrotic leaves. Ginkgo leaf necrosis is a common sight in areas where typhoons frequently occur, especially along the coast, where gingko leaves show smaller NDVIr values. Salisbury (1805) noted that great leaf injury oc- curred when rain was not associated with strong wind. The rainless or low-rainfall period during and after Typhoon 0613 reveals that the ginkgo leaf necrosis in Yamaguchi City is just like Salisbury's note.
Acknowledgements
This study was performed at the Research Labo- ratory of Environmental Ecology, Faulty of Agricul- ture, Yamaguchi University. We would like to express our gratitude to all members who helped our measure- ment of spectral reflectance.