1. Introduction
Population growth leads to an accelerated change from a natural environment to an urban landscape; therefore, it is advisable to conserve and increase vegetation through the creation of a greater number of urban green areas (UGAs) [
1,
2,
3]. The most important vegetation in UGAs are trees, as they provide a wide range of environmental, ecological and social services [
4,
5,
6]. However, urban trees face stressful conditions due to factors such as the heat island effect, soil compaction, limited growth space for roots, vandalism, inadequate management practices, and water and nutrient deficiency, among others [
7,
8,
9,
10]. The impact of stress on urban trees can be identified by observing the condition of their crowns. An alteration in their morphological characteristics negatively affects their vitality and general health condition, and also has an impact on the provision of services to the urban environment [
6,
11,
12,
13,
14,
15].
Tree crown assessment is used as an indicator of health condition in forest species, with some of these variables being crown density, crown transparency and dieback [
11,
16,
17]. Recently, these indicators have been adapted and used to estimate the health condition of urban trees; however, obtaining this information involves
in situ data collection by at least two people [
4,
6,
17,
18,
19], which entails a considerable expenditure of time and is complicated when access to the terrain is restricted or dangerous; currently, this method is frequently used to obtain information on tree health condition in both forest and urban areas [
4,
6,
10,
20]. On the other hand, there are methods to evaluate physiological processes to quantify the response of trees to stress, one of them being chlorophyll fluorescence (Fv/Fm). This index indicates the photosynthetic efficiency of the system of the leaves; thus, a lower efficiency is related to a lower health condition of the vegetation [
21,
22].
However, a feasible method for studying tree crowns is the use of unmanned aerial vehicles (UAVs), since being equipped with high-resolution multispectral sensors allows obtaining precise information from large areas and reducing the time necessary for the analysis of various biophysical parameters compared to traditional methods [
9,
20,
23,
24,
25,
26,
27]. Recent vegetation studies have made use of spectral bands to determine vegetation indices (VIs), among other applications; this remote sensing technology allows classifying and estimating health condition of vegetation in different ecosystems, as well as in urban areas [
28,
29,
30,
31]. Among the vegetation indices used in research are the normalized difference vegetation index (NDVI), the enhanced vegetation index (EVI2), the green normalized difference vegetation index (GNDVI), the blue normalized difference vegetation index (BNDVI), the red-green-blue vegetation index (RGBVI), and the green-red vegetation index (GRVI) [
5,
9,
20,
26,
32,
33,
34,
35].
Vegetation indices have advantages over other methods, e.g., NDVI has a better correlation with tree canopy cover than with other ground-level vegetation covers, and high NDVI values indicate healthy vegetation conditions [
2,
34]. High GNDVI values effectively represent chlorophyll properties, while BNDVI allows the spatial distribution of chlorophyll to be analyzed [
26,
32,
36]. These characteristics allow analyzing different options in determining the condition of the trees. Therefore, the aim of this study was to determine the degree of correlation between the absolute variables crown density, crown transparency, and dieback of trees located in urban green areas with the vegetation indices NDVI, EVI, BNDVI, GNDVI, GRVI, and RGBVI, as well as chlorophyll fluorescence with the purpose of identifying more efficient predictors of tree health condition.
4. Discussion
The smaller diameters and heights of the evaluated trees (
Figure 4) indicate that the species may be mostly young (
Figure 4A) [
20]. It was also found that they are short (
Figure 4B), which may be due to pruning activities on the tree crowns. The result is contrary to what was found, for example, in the city of Montemorelos, Nuevo León, Mexico, where the urban trees are larger [
52], which may indicate that cultural practices are an important factor affecting the structure and composition of tree vegetation in urban areas. On the other hand, older trees would be expected to have crowns with high density (Cdn) values and low percentages of crown transparency (Ctr) and dieback (Cdie); however, maintenance actions carried out on the crowns (formation pruning) alter their shape and condition, diminishing the vitality of the trees and in extreme cases leading to their death [
6,
20].
In general, trees are considered healthy when they present values of Cdn > 50 %, Ctr < 30 % and Cdie < 5 % (Saavedra-Romero
et al., 2016). The values of Cdn, Ctr and Cdie found in the trees located in the 21 UGAs of the city of Texcoco have average values of 67.96 % in Cdn, 35.19 % in Ctr and 1 % in Cdie (
Figure 5). A high crown density value indicates that the tree has a large number of leaves, which translates into greater photosynthetic capacity and therefore better growth and development [
9,
14]. In contrast, a low Cdn value translates into little foliage, which can result in physiological stress and greater susceptibility to pest and disease attack [
20,
46]. As for Ctr, it showed values above 30 % (
Figure 5B), indicating that these trees are under stress; however, an annual monitoring of the increase in crown transparency in the trees would help to determine if their growth is compromised, indicating medium-term damage to their reproductive potential and long-term consequences for their survival. Cdn and Ctr can vary by species, age, genotype and evaluation periods. Despite this, at present, these variables are widely used as useful indicators in the evaluation of tree crown condition in both natural and urban environments [
6,
22]. Regarding Cdie, it presented lower frequency within the trees in the 21 UGAs evaluated (
Figure 5C). Trees with high Cdie values generally exhibit poor structural conditions, an irregular crown shape and little foliage; therefore, a value higher than 5 % in Cdie would indicate that they are not healthy trees [
6,
14]. The urban environment is a stress factor for trees, with a lack of water being one of the factors present in urban areas and which mainly affects variables such as Cdie [
4,
6]
One way of estimating the vitality of vegetation is based on the amount of chlorophyll present in its leaves, with the use of multispectral images having become a fast and low-cost alternative for estimating chlorophyll content [
48]. This work found that NDVI correlated positively with Fv/Fm (
Figure 6), given that chlorophyll fluorescence evaluates the photosynthetic activity of the leaves and NDVI is sensitive to chlorophyll. An association was found between these variables which can help to better evaluate the condition of the tree crown than other type of indices. This is due to the polyfunctionality of NDVI and good results achieved in different environments; it also serves as a point of comparison with other indices [
2,
34,
53]. On the other hand, a low correlation may be due to several reasons; one that has been studied recently is the flowering phenology that interferes with the spectral bands, that is, the degree and variety of colors present in the flowers that alter the "greenness" recorded by the index and that may vary according to the time of the year in which it is evaluated [
24,
36]. BNDVI instead showed a lower correlation with Fv/Fm (
Figure 6), despite the fact that this index helps in the analysis of spatial heterogeneity and chlorophyll distribution; in contrast, a study on bryophytes found a positive correlation between BDNVI and Fv/Fm, which is attributed to the characteristics of the vegetation studied (non-vascular plants), as well as the diversity of species studied [
32,
54].
Another evaluated vegetation index which is an indicator of the greenness of the tree canopy is the GNDVI; in this case it did not show a significant correlation with Fv/Fm (
Figure 6), possibly due to the same flowering condition mentioned above. However, a study on the species
Coffea arabica found that some of the indicators related to the leaf content (chlorophyll) of this species were NDVI and GNDVI [
48]; it should also be noted that GNDVI has recently been used to estimate the floral proportion in tree crowns located in natural forests at the pixel level with an accuracy > 85 % [
36]. In this case, it is important to point out that among the tree species that flowered to different degrees during the study were
Bauhinia variegata L. (pink, purple, and white flowering),
Spathodea campanulata P.Beauv. (orange flowering),
Talipariti tiliaceum (L.) Fryxell (pink and yellow flowering),
Jacaranda mimosifolia D Don. (purple flowering) and
Grevillea robusta A. Cunn. ex R. Br. (yellow and orange flowering), of which only jacaranda was among the most frequent species in the UGA. Although the correlations between Fv/Fm and the vegetation indices were low, it is also important to note that significant statistical differences were found (p < 0.05).
On the other hand, the correlations between Fv/Fm with Cdn and Ctr (
Figure 6) indicate a reference to the health condition of the trees, since it is known that the presence of sparse crowns or those with high percentages of transparency are indicative of stress, which can be evaluated through Fv/Fm [
22,
50]. Fv/Fm is widely used in crop analysis; however, its use has rapidly spread to other natural and non-natural environments, so it is also used in urban tree stress assessment [
32,
49]. For example, some studies have detected stress in tree plant species through Fv/Fm under various cultural practices within UGAs, which include management and maintenance activities, particularly crown pruning or transplanting of urban trees [
6,
22,
49]. Finally, NDVI and BNDVI were found to correlate with Cdn and Ctr, this given that they use a similar mathematical relationship [
48]; however, crown variables are better related to NDVI.
The association between indices, such as the high correlation found between BNDVI and GNDVI (
Figure 6), indicates that the variability not explained by one index can be explained by the other, and, therefore, they complement each other [
26,
32]; this allows the development of predictive models [
48]. In this sense, the regressions between crown variables and vegetation indices showed associations between NDVI, BNDVI, Cdn and Ctr, which have been described in other studies [
9,
26,
34,
55]; one of the most noteworthy is NDVI with tree density and r
2 values greater than 0.7. This indicates that with these data it is possible to generate predictive models [
28]. With the growth of urban areas and the incorporation of various artificial elements, the generation of predictive vegetation index models with greater accuracy becomes essential. In this sense, a study classified vegetation using NDVI, GNDVI, BNDVI, RGBVI, GRVI and SAVI (Soil Adjusted Vegetation Index) and developed an index that discriminates urban elements such as steel roofs and waterproofing, among others, when these predominate in the images [
26].
The CV revealed instead that there are differences between high and low values of the indices (
Figure 8). The results suggest that the evaluation of chlorophyll (green color) is not uniform with low values of the indices, which may be caused by some anthropogenic damage [
35,
48]. Studies on crops such as coffee (
Coffea arabica L.), in which various plant indices are evaluated in diseased and healthy leaves, indicate that a high CV may represent a non-uniform distribution of chlorophyll for diseased leaves and this may be due to various factors that cause the degradation of the pigment (chlorophyll), such as trauma, chemicals, infectious agents, and senescence stages, among others [
28,
48].
Author Contributions
Conceptualization, L.M.M.-G., T.M.-T. and L.L.S.-R.; methodology, L.M.M.-G., T.M.-T., P.H.-R., D.A.-R., A.G.-G.; validation, L.M.M.-G., T.M.-T., and P.H.-R.; formal analysis, L.M.M.-G., T.M.-T., D.A.-R. and P.H.-R.; investigation, L.M.M.-G., T.M.-T., D.A.-R. and L.L.S.-R.; writing—original draft preparation, L.M.M.-G., T.M.-T. and A.G.-G.; writing—review and editing, L.M.M.-G., T.M.-T., D.A.-R., P.H.-R. and L.L.S.-R.; visualization, L.M.M.-G. and T.M.-T.; supervision, T.M.-T., D.A.-R., and P.H.-R.; project administration, L.M.M.-G. and T.M.-T.; funding acquisition, L.M.M.-G. and T.M.-T. All authors have read and agreed to the published version of the manuscript.
Figure 1.
Location of green areas in the city of Texcoco de Mora.
Figure 1.
Location of green areas in the city of Texcoco de Mora.
Figure 2.
Example applied to the six evaluated indices and 21 UGAs studied. (a) Location of the tree species under study prior to sampling. (b) Digitization of crowns. (c) Calculation of the vegetation index. (d) Extraction of pixel values of each tree’s crown index.
Figure 2.
Example applied to the six evaluated indices and 21 UGAs studied. (a) Location of the tree species under study prior to sampling. (b) Digitization of crowns. (c) Calculation of the vegetation index. (d) Extraction of pixel values of each tree’s crown index.
Figure 3.
Methodological diagram of the study.
Figure 3.
Methodological diagram of the study.
Figure 4.
Diameter (A) and height (B) categories in 549 trees located in UGAs in the city of Texcoco de Mora.
Figure 4.
Diameter (A) and height (B) categories in 549 trees located in UGAs in the city of Texcoco de Mora.
Figure 5.
Histograms of frequencies and cumulative frequencies for the variables crown density (Cdn), crown transparency (Ctr) and dieback (Cdie) in UGAs in the city of Texcoco de Mora.
Figure 5.
Histograms of frequencies and cumulative frequencies for the variables crown density (Cdn), crown transparency (Ctr) and dieback (Cdie) in UGAs in the city of Texcoco de Mora.
Figure 6.
Pearson correlation matrix (r) between vegetation indices, chlorophyll fluorescence and tree variables (p < 0.05). FvFm: chlorophyll fluorescence, NDVI: Normalized difference vegetation index, EVI: Enhanced vegetation index, BNDVI: Blue normalized difference vegetation index, GNDVI: Green normalized difference vegetation index, GRVI: Green-red vegetation index, RGBVI: Red-green-blue vegetation index, Cdn: Crown density, Ctr: Crown transparency, Cdie: Crown dieback, Dbh: diameter at breast height and Th: Total height.
Figure 6.
Pearson correlation matrix (r) between vegetation indices, chlorophyll fluorescence and tree variables (p < 0.05). FvFm: chlorophyll fluorescence, NDVI: Normalized difference vegetation index, EVI: Enhanced vegetation index, BNDVI: Blue normalized difference vegetation index, GNDVI: Green normalized difference vegetation index, GRVI: Green-red vegetation index, RGBVI: Red-green-blue vegetation index, Cdn: Crown density, Ctr: Crown transparency, Cdie: Crown dieback, Dbh: diameter at breast height and Th: Total height.
Figure 7.
Adjusted R2 of the linear regressions between the five most frequent tree species in the study area, crown indicators and vegetation indices evaluated. LL: Ligustrum lucidum W. T. Aiton; JM: Jacaranda mimosifolia D. Don; FU: Fraxinus uhdei (Wenz.) Lingelsh.; CS: Cupressus sempervirens L.; CL: Cupressus lusitanica Mill.; NDVI: Normalized difference vegetation index; EVI: Enhanced vegetation index; BNDVI: Blue normalized difference vegetation index; GNDVI: Green normalized difference vegetation index; GRVI: Green-red vegetation index; RGBVI: Red-green-blue vegetation index; Cdn: Crown density; Ctr: Crown transparency; and Cdie: Crown dieback.
Figure 7.
Adjusted R2 of the linear regressions between the five most frequent tree species in the study area, crown indicators and vegetation indices evaluated. LL: Ligustrum lucidum W. T. Aiton; JM: Jacaranda mimosifolia D. Don; FU: Fraxinus uhdei (Wenz.) Lingelsh.; CS: Cupressus sempervirens L.; CL: Cupressus lusitanica Mill.; NDVI: Normalized difference vegetation index; EVI: Enhanced vegetation index; BNDVI: Blue normalized difference vegetation index; GNDVI: Green normalized difference vegetation index; GRVI: Green-red vegetation index; RGBVI: Red-green-blue vegetation index; Cdn: Crown density; Ctr: Crown transparency; and Cdie: Crown dieback.
Figure 8.
Differences in the coefficient of variation (CV) between High (> 3rd Quartile) and Low (< 3rd Quartile) values of the evaluated vegetation indices (p < 0.05). NDVI: Normalized difference vegetation index; EVI: Enhanced vegetation index; BNDVI: Blue normalized difference vegetation index; GNDVI: Green normalized difference vegetation index; GRVI: Green-red vegetation index; and RGBVI: Red-green-blue vegetation index.
Figure 8.
Differences in the coefficient of variation (CV) between High (> 3rd Quartile) and Low (< 3rd Quartile) values of the evaluated vegetation indices (p < 0.05). NDVI: Normalized difference vegetation index; EVI: Enhanced vegetation index; BNDVI: Blue normalized difference vegetation index; GNDVI: Green normalized difference vegetation index; GRVI: Green-red vegetation index; and RGBVI: Red-green-blue vegetation index.
Table 1.
Urban green areas in Texcoco de Mora, State of Mexico, Mexico.
Table 1.
Urban green areas in Texcoco de Mora, State of Mexico, Mexico.
ID |
Name |
Perimeter (m) |
Area (m2) |
A |
Boulevard Jiménez Cantú |
940.53 |
4,687.21 |
B |
Valle de Santa Cruz 2 |
141.72 |
848.98 |
C |
Jardín San Martín |
259.84 |
1,379.92 |
D |
Parque Niños Héroes |
205.03 |
2,632.24 |
E |
Parque las Américas |
174.75 |
1,123.34 |
F |
Parque del Ahuehuete |
132.96 |
876.11 |
G |
Parque Heberto Castillo |
304.93 |
4,167.78 |
H |
Parque Arteaga |
92.05 |
435.07 |
I |
Parque de la Tercera Edad |
406.05 |
9,478.5 |
J |
Jardín Municipal |
549.66 |
9,765.82 |
K |
Valle de Santa Cruz 3 |
118.35 |
717.83 |
L |
Valle de Santa Cruz 1 |
192.78 |
2,128.93 |
M |
Parque Municipal |
366.93 |
2,694.09 |
N |
Alameda Texcoco |
849.57 |
43,898.99 |
O |
Parque Xolache |
517.07 |
7,436.39 |
P |
Camellón Lechería |
2,505.49 |
7,554.33 |
Q |
Deportivo Silverio Pérez |
765.46 |
37,159.45 |
R |
Parque Bicentenario |
859.26 |
21,397.46 |
S |
Boulevard Chapingo |
2,801.45 |
16,347.42 |
T |
Las vegas 1 |
151.56 |
1,105.62 |
U |
Las vegas 2 |
167.91 |
1,173.21 |
Table 2.
Equations used to determine vegetation indices.
Table 2.
Equations used to determine vegetation indices.
Formulas |
Where |
NDVI |
NDVI = Normalized difference vegetation index Nir = Near infrared Red = Red band |
EVI2 =
|
EVI2 = Enhanced Vegetation Index Nir = Near infrared Green = Green band |
GNDVI=
|
GNDVI = Green normalized difference vegetation index Nir = Near infrared Green = Green band |
BNDVI=
|
BNDVI = Blue normalized difference vegetation index Nir = Near infrared Blue = Blue band |
GRVI = |
GRVI = Green-red vegetation index Red = Red band Green = Green band |
RGBVI= |
RGBVI = Red-green-blue vegetation index Red = Red band Green = Green band Blue = Blue band |
Table 3.
Average of forest measurement variables for the 10 most frequent species in UGAs in the city of Texcoco de Mora.
Table 3.
Average of forest measurement variables for the 10 most frequent species in UGAs in the city of Texcoco de Mora.
Species |
# of trees |
Diameter (cm) |
Height (m) |
Cupressus lusitanica Mill. |
53 |
24.76bc
|
6.84bc
|
Fraxinus uhdei (Wenz.) Lingelsh. |
48 |
25.57bcd
|
7.38ab
|
Jacaranda mimosifolia D. Don |
44 |
22.38de
|
7.46b
|
Cupressus sempervirens L. |
41 |
13.54e
|
6.92b
|
Ligustrum lucidum W.T. Aiton |
40 |
16.39cde
|
4.94d
|
Ficus microcarpa L.f. |
38 |
20.60bcd
|
6.27bc
|
Cupressus macrocarpa Hartw. |
38 |
15.40de
|
5.20cd
|
Schinus molle L. |
31 |
52.65a
|
8.40a
|
Casuarina equisetifolia L. |
28 |
28.26b
|
9.38a
|
Ficus benjamina L. |
27 |
21.53bc
|
4.53d
|