Introduction

The surveys made in urban green areas confirm that the decisions of major impact on forest health are planting density and species selection. In cities, the chronic exposure to air pollution, damages linked to vandalism and the incorrect planting sites are factors reducing tree vitality and make it vulnerable to pests and diseases (^{Smiley et al., 2006}; ^{Tiddens and Cloyd, 2006}; ^{Chacalo and Corona, 2009}; ^{PAOT, 2010}; ^{Koeser et al, 2013}).

In an area classified as urban land, 630 km², in Mexico City, it is estimated that the percentage of green areas may be declining at a rate of 3.7 % per year. This implies a reduction of the social and economic value of the woodland component without which the financial investment in the management and maintenance of the parks is not justified, leading to a gradual deterioration of its health, a crucial aspect in the field of arboriculture and urban forestry. It would seem, then, that the trees are perceived more as a problem than as an economic good, so the option is to remove them frequently, but without replacement (^{Chacalo et al, 1994}; ^{McPherson, 2007}; ^{Chacalo and Corona, 2009}).

Forest health has focused on analyzing the biotic and abiotic factors that affect the vigor and productivity, and are exhibited through symptoms in the structures that make up the tree. In this context, urban trees, the greatest impact comes from pests and pathogens and abiotic damage (chemical physical, and mechanical elements) that affect their development, and that must be considered first if any problems are detected in the woodland. For example, in the United States of America damages of this sort were associated to losses of up to 20 % in some stands as they predisposed trees to the attack by disease on the site (^{Boa, 2003}; ^{Cibrián et al., 2007}).

By the "damage to trees" indicator, the type, location and severity of damage caused by disease, pests, weather events and human activities can be assessed (^{FIA, 2002}; ^{FIA, 2012}; ^{INFyS, 2012}). It is important because with this information related investigations in field-specific detection of the causative agents are promoted, in addition to specify the role of biotic and abiotic factors and influences as stressful processes inherent to the forest ecosystem. In this paper the methodology of this indicator was applied, with modifications to urban areas, to identify and classify the major health problems, distribution and severity in the woodland of three parks in Mexico City.

Materials and Methods

The study sites were three parks in the urban area of Mexico City: Alameda Oriente (19°26'7.63" N - 99° 03'18.53" W) in Venustiano Carranza; Alameda Norte (19°30'4.25" N - 99°10'41.08" W) in Azcapotzalco and Alameda Sur (19°18'32.70" N - 99°7'22.29" W) in Coyoacán (Figure 1). These parks are characterized by their free or little restriction access to users and are adjacent to avenues and streets of intense and constant traffic.

Figure 1 Parks of Mexico City where tree damage assessment was made. 

Clusters of four circular plots were established in the form of an inverted Y, according to the INFyS and FIA methodology (^{FIA 2002}; ^{FIA, 2012}; ^{INFyS, 2012}), which was adjusted for urban areas; each plot had a single area of 408.30 m² and a radius of 11.4 m (^{Nowak, 2006}; ^{I-Tree, 2010}; ^{FIA, 2012}; ^{INFyS, 2012}) and sampling and re-measurement were made in them. In Alameda Norte a total area of 8 166 m² (five clusters) were evaluated and in Alameda Oriente and Sur, 6 532 m² (four clusters each). Three samples were taken in spring-autumn (May-October, 2011) and one in winter (November, 2011-January, 2012). All trees within each plot were numbered, were identified by species and evaluated according to the parameters of the indicator of damage.

Up to two damage symptoms were recorded per tree. From the most likely to occur, codes for fast data were developed, as the location of the injury, severity (according to pre-established thresholds) and forest species identified as most affected were recorded as well (^{Alvarado et al, 2012}).

The "no harm" category applies to the healthy trees or damages whose severity was below the threshold. The calculated value for the Damage Severity Index (DSI) per cluster was performed with the formula:

DSI= Nature of the causing agent x Harm localization code

which uses data of the kind of damage, localization (Figure 2) and severity (Tables 1 and ²)

Figure 2 Places of tree damages. 

Table 1 Factors for the calculation of the Damage Severity Index (DSI) in the trees of the study sites. 

Table 2 Factors for the calculation of the Damage Severity Index (DSI) with parasitic plants in the trees of the study sites. 

For damages related to parasitic plants, the following formula was used:

DSI= Nature of the causing agent x Harm localization + Severity

The code for the nature of the causing agent is assigned from the damage that occur in roots and trunk, which are considered the most serious (^{FIA, 2002}).

Data were analyzed for frequency distributions, Mode values and percentiles to determine the damages of the highest incidence by site as well as the number of occurrences within each cluster and its relation to the tree identified species. The SPSS programs for Windows 15.0 version (^{SPSS, 2006}) and the 10.2.2 ArcMap (^{ArcGis-ESRI, 2014}) were used.

Results and Discussion

In the three evaluated sites were found healthy, damaged and dead standing trees. To explain the impact of each one of them, the mode was calculated, as it represents the most common value in a data distribution (^{Cochran, 2008}). The category named "undamaged" recorded the highest in the three parks, which suggests the prevalence of healthy individuals, but also a large number with symptoms below the thresholds.

The main problems identified in the three sites were related with vandalism in its various forms (paint on trees, garbage accumulation, injuries and intentional injuries in branches and roots). In urban forestry, the percentage of damaged trees is calculated to estimate the environmental, economic and social benefits that each tree or group of trees represent, which decreases under the influence of damage on differences in size, growth rates, foliage features and even the location of trees within the urban area (^{McPherson and Simpson, 2002}).

According to data analysis (75^th percentile), 75 % of woodland in the Alameda Norte showed involvement by sucking insect Stenomacra marginella in spring and summer; at Alameda Oriente, the same percentage had symptoms related to vandalism while in the Alameda Sur the same proportion of trees showed some type of disturbance in the foliage (mistletoe, discolorations, blemishes, burns) in the fall and winter samples (Table 3). Inadequate planting conditions were also observed, in which space is limited for the optimal development of forest species; then the roots are blocked, the stems do not develop, and from overlapping canopies, trees do not get enough light to fully perform photosynthesis and other vital functions (^{Loh et al., 2003}; ^{Tovar, 2007}; ^{Chacalo and Corona, 2009}; ^{Koeser et al., 2013}).

Table 3 Major damages identified in the studied sites in Mexico City (2011-2012). 

Sampling 1 = May 2011; Sampling 2 = August 2011; Sampling 3 = October 2011; Sampling 4 = January 2012

Damages caused by vandalism (the wounds on the stems in particular) function as inputs for pathogens such as fungi, or sucking and boring insects and is usual in urban green areas (^{Martínez, 2008}).

In the cities, the greatest impacts on the environment occur from the change in land use and urbanization, so it is very common to believe that only the anthropogenic factors influencing health status of the woodland (^{Cibrián et al., 2007}). In the three parks, unfavorable conditions for the development of trees as high density planting, nutrient-poor soil, compacted soil, anthropogenic damage, poor maintenance (irrigation and fertilization) and chronic exposure to air pollutants were detected, reducing its force and makes them more susceptible to pests and diseases that are normally secondary (^{Cibrián et al., 2001}; ^{Boa, 2003}; ^{Smiley et al., 2006}; ^{Tiddens and Cloyd, 2006}; ^{Chacalo and Corona, 2009}; ^{Koeser et al, 2013}). This susceptibility is visible with the high incidence of parasitic plants and sucking insects recorded in each sampling and remeasurement.

At all three sites the presence of parasitic plants of the Cladocolea and Strutanthus genera was recorded, and the most important element in urban areas is the severity of the attack, as it has been estimated that 83 of every 100 trees in the city could be infested with these organisms, and that at least 53 % of them have a level of severe damage. This becomes worse when considering that out of the 68 of the most common tree species of the in green areas of the City, 95 % are susceptible to colonization by some kind of mistletoe. In the Alameda Norte and Alameda Sur the incidence of parasitic plants was detected mainly in Populus tremuloides Michx., P. alba L. and Acer negundo L. with a progressive decline of the trees from partial to total loss of foliage, deformation of the cups by severe phytosanitary pruning (Alameda Sur) to the removal of dead standing trees (Table 4).

Table 4 Major damages recorded in the studied sites in Mexico City (2011-2012). 

F_i(n) = Absolute frecuency; Fr_i(n) = Relative frecuency; nr = Not in record.

This vulnerability in urban trees is related to site conditions in which they survive: chronic stress, poor fertilization, low water availability, vandalism and pollution (^{De la Paz et al, 2006}; ^{Sandoval and Gutiérrez, 2006}; ^{García, 2008}; ^{Martínez, 2008}; ^{Alvarado, 2012}). This confirms the widespread problem of forest health that makes controlling these abiotic factors a priority in management programs in the delegations of Mexico City.

In Alameda Norte were detected trees with twisted roots ("pigtail") resulting from wrong planting and, as some disease in this structure, they lead to slower growth of tree height, diameter, leaf size, dieback and root development (^{Cibrián et al., 2007}).

In Alameda Oríente traces of the presence of Glycaspís brímblecombeí and woodpeckers were also found. Additionally, the combination of the high density of plants and the low restricted access to the facilities, contribute to tree weakening and important loss of foliage (^{PAOT, 2011}).

In Alameda Sur vandalism-related damage was identified, but also S. margínella was detected in the first two samplings in all the clusters evaluated. In its adult form, this sucking insect is found from late winter to mid-summer when it feeds on the foliage thus affecting its quality and weakening the tree (^{Cibrián et al., 2000}).

Without proper planning, the effective management of health problems will depend on the early recognition of the symptoms from the responsible staff of each park.

Location of damage

With respect to the structures most affected in the Alameda Norte and the Alameda Oríente localized damage in the shaft associated with vandalism and sucking insects (S. margínella). In the Alameda Sur they were mainly identified in the foliage and are associated with parasitic plants and water deficit. In the three sites it is considered as a specific case the assessment of Fraxínus uhdeí and Ulmus parvífolía Jacq., in regard to the time of sampling in August and September when changes in the color of foliage (green to red, purple and yellow) are common, as they are deciduous. F. uhdeí loses its leaves in short periods during the dry season; as it is sensitive to ozone, sucking insects, availability of water, soil compaction and pollution (^{Cibrián et al., 2001}; ^{Conabio, 2011}), it is important to compare samples in different seasons to differentiate damage from normal physiological processes (Figure 3).

Figure 3 Location of tree damage of the three parks studied in Mexico City. 

Severity Index

According to individual calculations, in Alameda Norte DSI values did not differ between the first and the last sampling, with a range of medium to high in areas where there were conditions of high competition for space and light. DSI average values were associated with suppressed trees (Figure 4). In the Alameda Oríente the lowest figures of the three sites were obtained, with increases in low to medium in park areas with higher density planting with trees in decline (Figure 5). Alameda Sur was the only place we saw a dramatic increase in values DSI medium to high by increasing the number of trees classified as "very damaged/dead standing" at the end of the evaluation period (Figure 6). Many of these trees were infested by parasitic plants.

Figure 4 Calculated Damage Severity Index (DSI) in the Alameda Norte , Mexico City. 

Figure 5 Calculated Damage Severity Index (DSI) in the Alameda Oriente , Mexico City. 

Figure 6 Calculated Damage Severity Index (DSI) in the Alameda Sur , Mexico City. 

High values of DSI indicated more than one tree damage, a severe one according to the causal agent and the threshold, or a widespread one. Carriers of minimum damages in a group or stand can still be classified as in good health. DSI results are usually analyzed on the basis of the forest species that is involved by interspecific biological differences (^{FIA, 2002}).

In the three study sites, A. negundo and F. uhdeí recorded higher values in regard to Casuarína equísetífolía L., which was related to the high susceptibility of the first to the incidence of parasitic plants. This abundance in Alamedas Norte and Sur explains that the abundance of trees in decline or dead standing has been greater at the end of the evaluation (Figure 7).

Figure 7 Damage Severity Index (DSI) in the three studied sites of Mexico City. 

When calculating the values in question, it was established that for the "nature of the causal agent" factor is considered that those that affect the roots and stem are more important because they affect the entire tree, while the damage to their peripheral parts can be temporary because the leaves, buds and reproductive structures are replaced or are conditioned by the season and the processes inherent to individuals (^{Alvarado and Saavedra, 2011}).

Conclusions

The three sites are studied have free or restricted access to visitors, therefore, a widespread distribution of damage was observed in clusters. The main identified symptoms in the trees are associated with vandalism and parasitic plants, most of which are on the stem and foliage, respectively. The calculated DSI showed that the lowest values correspond to specimens with minimal damage, while high numbers relate to those which are in the process of decline as a result of both, biotic and abiotic factors. The application of the methodologies of the indicator was useful for obtaining reliable data quickly and in a practical way, especially in a constantly changing environment as in Mexico City. The presence of damage indicates that the group of stressing agents impact the life of the tree, and can reduce it to one or two years as well as its growth in the short term, and on the other hand, to affect in a negative way, the social and environmental benefits that they provide the city.

Conflict of interests

The authors declare no conflict of interests.

Contribution by author

Alejandra Yunuen Zaragoza Hernández: discussion of the topic, implementation of the Project, data taking, data analysis and writing of the manuscript; Víctor Manuel Cetina Alcalá: discussion of the topic, review of concepts and writing of the manuscript; Miguel Ángel López López: discussion of the topic, review of concepts, data analysis and review of the manuscript; Alicia Chacalo Hilú: discussion of the topic, review of concepts and methodology, data analysis and review of the manuscript; María deLourdes de la Isla de Bauer: review of concepts, data analysis, review of literature and writing of the manuscript; Dionicio Alvarado Rosales: discussion of the topic, review and implementation of the methodology, data taking and review of the manuscript; Héctor González Rosas: discussion of the topic review of concepts and literature, and the manuscript.