¹Facultad de Ciencias Agrícolas campus Xalapa, Universidad Veracruzana. México.

²Red de Ambiente y Sustentabilidad, Instituto de Ecología, A. C. (Inecol). México.

Urban air pollution places chronic stress on trees through the deposition of pollutants from human activities, including metals associated with vehicle and industrial emissions, which can disrupt physiological processes and affect plant growth. Although metal accumulation in leaves has been used as a biomonitoring tool, gaps remain in the understanding of its relationship to morphological and growth changes in dominant urban species. Within this context, the present study evaluated the concentration of metals on the leaf surface and the fraction absorbed by the tissue, as well as the nutrient content in the leaves of the ash tree (Fraxinus uhdei), a species widely distributed in urban forests in the Mexico City Metropolitan Area (ZMVM in Spanish). The analysis was conducted in three urban forests with contrasting environments. The concentrations of surface and absorbed metals and the nutrient content were determined, and their associations with morphological and growth variables were evaluated using multiple linear regression (stepwise method) and nutrient vector analysis. The results showed that copper (both surface and absorbed) was positively associated with increased leaf area, whereas metals of anthropogenic origin, such as lead, cadmium and chromium were negatively associated with increased diameter. The nutritional analysis revealed negative correlations between leaf biomass and nutrient concentrations. These findings suggest that the accumulation of metals in tree foliage may influence the physiology and nutrition of urban trees and provide a basis for their monitoring and management.

Keywords: Metal uptake, leaf biomass, leaf biomonitoring, urban forests, trace metals, plant nutrition.

La contaminación atmosférica urbana ejerce presión crónica sobre el arbolado, debido al depósito de contaminantes generados por actividades antropogénicas, entre ellos metales asociados a emisiones vehiculares e industriales que pueden alterar procesos fisiológicos y afectar el crecimiento vegetal. Aunque la acumulación foliar de metales se ha utilizado como herramienta de biomonitoreo, aún existen vacíos en la compresión de su relación con cambios morfológicos y de crecimiento en especies urbanas dominantes. En este contexto, en el presente estudio se evaluó la concentración de metales en la superficie foliar y la fracción absorbida por el tejido, así como el contenido de nutrimentos en hojas de fresno (Fraxinus uhdei), especie ampliamente distribuida en bosques urbanos de la Zona Metropolitana del Valle de México (ZMVM). El análisis se realizó en tres bosques urbanos con entornos contrastantes. Se determinaron las concentraciones de metales superficiales y absorbidos, y el contenido de nutrimentos, evaluando su asociación con variables morfológicas y de crecimiento mediante regresión lineal múltiple (método stepwise) y análisis vectorial nutrimental. Los resultados mostraron que el cobre (superficial y absorbido) se asoció positivamente con el incremento del área foliar, mientras que metales de origen antrópico como plomo, cadmio y cromo se relacionaron negativamente con el incremento del diámetro. El análisis nutrimental evidenció relaciones negativas entre la biomasa foliar y las concentraciones de nutrimentos. Estos hallazgos indican que la acumulación foliar de metales puede influir en la fisiología y nutrición del arbolado urbano y aportan bases para su monitoreo y manejo.

Palabras claves: Absorción de metales, biomasa foliar, biomonitoreo foliar, bosques urbanos, metales traza, nutrición vegetal.

Air pollution is one of the main environmental pressures in megacities, where emissions from vehicle traffic, industrial activity, and other urban sources generate high concentrations of particulate matter and trace metals (Molina & Molina, 2004). Within this context, urban vegetation plays a significant role by intercepting and trapping pollutants on leaf surfaces, which helps reduce airborne particles such as PM₁₀, PM_2.5, and PM₁, which carry metals; and as a result, air quality is improved (Lindén et al., 2023). However, this function involves continuous exposure to toxic substances that can accumulate and enter plant tissue, disrupting physiological processes such as photosynthesis, nutrient balance, and the growth of urban trees (Kabata-Pendias, 2010; Bierza & Bierza, 2024).

In the Mexico City Metropolitan Area (ZMVM, for its acronym in Spanish), vehicle and industrial emissions are major sources of trace metals in the urban atmosphere (Molina & Molina, 2004). In particular, transportation accounts for more than 50 % of total air pollutant emissions (Secretaría de Medio Ambiente de la Ciudad de México [Sedema], 2023). Recent studies have documented the accumulation of trace metals in the foliage of urban trees (Fonseca-Salazar et al., 2023; Sánchez-Landero et al., 2024), providing evidence of the direct exposure of species to these. However, several of these studies have focused on quantifying metal accumulation, while knowledge regarding its implications for leaf morphology, nutrient status, and the growth of urban trees remains limited.

This gap is significant for dominant species used in urban green spaces in the ZMVM, such as Fraxinus (Benavides-Meza et al., 2002), which has been cited as being relatively tolerant of air pollution (Catinon et al., 2008). Therefore, this study analyzed the surface and absorbed concentrations of metals and nutrients in the leaves of Fraxinus uhdei (Wenz.) Lingelsh. in three urban forests within the ZMVM that experience varying degrees of urban pressure. Their relationship with leaf morphological variables—leaf area, specific leaf area, and dry leaf weight—, as well as changes in diameter breast height (DBH), were also examined in order to provide evidence on the effects of air pollution on the functioning and growth of urban trees.

The study was conducted in three urban forests in the ZMVM with varying levels of anthropogenic pressure: (1) Naucalli Park (19°29’27.6” N, 99°14’21.2” W) North of the ZMVM, characterized by industrial activity; (2) Section 1 of the Chapultepec Forest (19°23’40” N, 99°10’40” W), located in the downtown area, with heavy traffic, and (3) the Tlalpan Forest (19°17’38.2” N, 99°11’36.3” W), to the South, with greater tree cover and lower urban density (Figure 1). The sites were selected based on the presence of Fraxinus uhdei and because they represent a spatial gradient of human pressure in urban green spaces within the ZMVM.

A linear transect of approximately 750 m was established for each forest, taking into consideration urban constraints such as infrastructure, sports facilities, and restricted-access areas. A systematic sampling method with a random starting point was utilized, selecting one mature and apparently healthy F. uhdei tree every 50 m up to a total of 15 individuals per site (total n=45 trees). When there were multiple eligible individuals at a sampling point (±8 m, GPS accuracy), one was selected by simple randomization (drawing lots); in inaccessible areas, the nearest tree was chosen while maintaining the spatial interval.

Leaves were collected from the canopy at a height of 7 m throughout the four seasons to determine surface and absorbed concentrations of metals and nutrients. Growth was estimated based on the increase in diameter at breast height (DBH) measured over three consecutive years using a 320-cm Forestry Suppliers Tape^® (accuracy ±1 mm). The soil pH was assessed for each tree at 30 cm deep in April, June and September, using a model 210 Hanna^® pH potentiometer, according to AS-02 method of the Mexican Official Standard NOM-021-RECNAT-2000 (Secretaría de Medio Ambiente y Recursos Naturales [Semarnat], 2002), in view of its influence on the availability and mobility of metals and nutrients in the soil-plant system.

The leaf area (LA) was determined for 100 leaves per tree using a model Li-3100C Li-cor^® leaf area meter, with the same method applied consistently across all individuals and sites. The leaves were collected from the middle third of the canopy; they were mature leaves with no visible damage, in order to standardize their physiological condition and minimize effects associated with age or position within the canopy. They were then dried at 75 °C until they reached a constant weight (model FE-291 Felisa^® drying oven), and the specific leaf area (SLA) was calculated using the method suggested by Pérez-Harguindeguy et al. (2013).

The concentrations of metals (Cu, Zn, Pb, Ni, Cr, Co, and Cd) were determined using 20 g of leaves per tree; each tree constituted a sample unit. The surface fraction of metals was obtained by washing with a disodium EDTA desorbing solution (disodium ethylenediaminetetraacetic acid; Na₂EDTA J. T. Baker^®, USA; lead-EDTA molar ratio=0.12) (Olguín et al., 2005). The leaves were then rinsed with deionized water, and the resulting solutions were analyzed using a model 3000 PerkinElmer^® inductively coupled plasma (ICP) spectrometer. To determine the absorbed concentration, the washed leaves were dried at 75 °C to constant weight (model FE-291 Felisa^® drying oven), ground in a GI^® mill, and sieved to 2 mm. Next, 0.25 g of the sample was digested with 6 mL of nitric acid (HNO₃) in a microwave digestion system, diluted in 25 mL of deionized water, filtered through Whatman^® No. 45 ash-free filter paper, and analyzed by ICP.

The concentrations of phosphorus (P) and potassium (K) were determined in the leaf material used for metal analysis; the same digestion and ICP analysis procedures were used. Nitrogen (N) was quantified in this plant material using the micro-Kjeldahl method, in accordance with the Association of Official Analytical Chemists International (Wendt-Thiex, 2023).

Differences among forests in LA, SLA, dry weight of the leaves (DW), and DBH growth were assessed using the Kruskal-Wallis and Mood-Median tests at a 95 % confidence level. The sampling unit was one tree (n=15 per site). First, the assumptions of normality (Shapiro-Wilk) and homogeneity of variances (Levene) were tested; since these assumptions were not met, nonparametric tests were applied.

The effect of metals (surface and absorbed), nutrients, and soil pH on leaf morphological variables and DBH growth was evaluated using multiple linear regression. The dependent variables considered were LA, SLA, DW, and increase in DBH, and the predictors were concentrations of metals, nutrients (N, P, and K), and soil pH. The analyses were conducted taking into account the location and the four seasons. Variables were selected using the stepwise procedure with forward selection and backward elimination to identify the predictors with the greatest explanatory power. The final models were selected based on the highest Coefficient of determination (adjusted R²) and significance (α=0.05), following an assessment of multicollinearity using the variance inflation factor (VIF). The analyses were performed using MINITAB^® version 14 (Minitab Inc., 2004). Finally, the nutrient balance of N, P and K was evaluated using vector nomograms, according to López-López and Alvarado-López (2010).

The Kruskal-Wallis test revealed significant differences among sites in SLA and in the increase in DBH (Table 1). The SLA recorded the highest median value in Tlalpan Forest, which could be attributed to its location in a less disturbed area. In environments with fewer disturbances, the availability of resources like water, light, and nutrients increases; this promotes higher SLA values and, consequently, higher tree growth rates (Poorter et al., 2009). The largest increase in DBH was found in the Naucalli Park, indicating variations in tree growth rates across sites. The literature indicates that local factors such as soil characteristics, site management, or the history of tree establishment can influence tree growth in urban environments (Pretzsch et al., 2017). However, these variables were not assessed in this study; therefore, the differences should be interpreted solely as inter-site variation.

LA = Leaf area; SLA = Specific leaf area; DW = Dry weight; DBH = Increase in DBH; M_e = Median. Identical letters indicate no significant differences between sites according to the Kruskal-Wallis test.

Table 2 shows the average surface and leaf tissue concentrations of Cu, Zn, Pb, Ni, Cr, and Cd in Fraxinus uhdei leaves, by site and season. At all three sites, Cu and Zn had the highest concentrations in both the surface and the absorbed fractions, while Ni had the lowest values. Cr, Cd, and Pb were detected in lower concentrations, although consistently, in the foliage of F. uhdei (Figure 2). The highest concentrations were observed in the spring and summer, suggesting greater accumulation during the growing season, when leaf growth promotes the interception of atmospheric particles over urban vegetation (Lindén et al., 2023).

Table 2. Average surface and absorbed concentrations of Cu, Zn, Pb, Ni, Cr, and Cd in Fraxinus uhdei (Wenz.) Lingelsh. leaves by site and season.

Forest	Metal	Spring		Summer		Fall		Winter
Forest	Metal	Surf.	Abs.	Surf.	Abs.	Surf.	Abs.	Surf.	Abs.
NP	Cu	14.3±6.1	13.6±5.8	17.90±7.7	16.7±7.3	7.1±3.6	0.004±0.001	5.5±2.0	0.01±0.01
	Zn	27.1±9.4	20.9±6.1	36.0±14.7	23.6±8.1	8.98±2.35	0.01±0.01	10.30±2.8	0.02±0.01
	Pb	0.2±0.16	Ud	2.23±2.25	0.04±0.01	0.05±0.01	0.001±0.001	1.98±2.5	0.01±0.001
	Ni	Ud	Ud	16.4±11.3	2.3±0.6	0.01±0.01	0.002±0.001	0.002±0.001	0.01±0.001
	Cr	0.52±0.23	0.2±0.17	1.66±1.21	0.84±0.57	0.001±0.001	0.001±0.00	0.28±0.61	0.01±0.001
	Cd	0.1±0.04	0.1±0.26	0.05±0.05	0.02±0.02	0.006±0.002	0.001±0.001	0.07±0.02	0.001±0.001
CF	Cu	11.37±6.5	8.32±6.01	10.6±5.07	5.96±1.91	5.52±3.03	0.01±0.01	6.79±3.26	0.02±0.02
	Zn	22.1±10.1	16.82±8.6	21.5±7.83	14.5±2.56	11.85±3.30	0.02±0.01	11.66±4.49	0.04±0.03
	Pb	0.58±0.53	Ud	0.26±0.27	Ud	0.01±0.01	0.01±0.01	4.69±4.34	0.01±0.01
	Ni	102.0±1.6	Ud	11.8±10.2	Ud	0.01±0.01	0.001±0.001	0.01±0.01	0.01±0.001
	Cr	1.17±1.07	0.19±0.19	0.53±0.27	0.34±0.02	0.01±0.01	0.01±0.001	1.0±0.6	0.001±0.001
	Cd	0.15±0.08	0.05±0.02	0.21±0.03	0.12±0.13	0.01±0.01	0.001±0.001	1.1±0.2	0.01±0.01
TF	Cu	7.59±3.79	7.59±3.79	11.8±6.76	7.8±4.0	4.17±1.05	0.02±0.01	4.77±1.96	0.01±0.001
	Zn	25.1±7.4	25.1±7.4	29.1±6.74	19.4±5.3	10.19±2.66	0.01±0.01	9.74±4.10	0.02±0.01
	Pb	Ud	Ud	0.42±0.42	0.10±0.01	0.001±0.01	0.001±0.001	1.8±2.7	0.01±0.001
	Ni	0.45±0.01	0.5±0.02	7.1±3.7	Ud	0.01±0.01	0.01±0.001	0.001±0.01	0.001±0.001
	Cr	0.32±0.01	Ud	0.57±0.52	Ud	0.001±0.001	0.001±0.001	0.07±0.10	0.01±0.001
	Cd	0.06±0.03	0.06±0.03	0.14±0.05	0.09±0.04	2.18±0.50	0.01±0.01	0.18±0.01	0.01±0.001

NP = Naucalli Park; CF = Chapultepec Forest; TF = Tlalpan Forest. Surf. = Surface; Abs. = Absorbed. Cu = Copper; Zn = Zinc; Pb = Lead; Ni = Nickel; Cr = Chrome; Cd = Cadmium; Ud = Undetermined; ± is the standard deviation. Concentrations are expressed in mg kg^-1.

Figure 2. Average surface and absorbed concentrations of Cd, Cu, Cr, Ni, Pb, and Zn in Fraxinus uhdei (Wenz.) Lingelsh. leaves by season.

The surface fraction is associated with the deposition of atmospheric pollutants on leaves, while the absorbed fraction reflects the uptake and translocation of these elements into plant tissues. This pattern has been documented in urban trees used as bioindicators of pollution, where Cu and Zn typically reach relatively high concentrations (3-14 mg kg^-1 and 20-90 mg kg^-1, respectively) due to their association with vehicle emissions, brake dust, and other urban sources (Rai, 2016; Youssef, 2020). The differences between fractions suggest that F. uhdei can accumulate metals both through surface deposition and through incorporation into leaf tissues. However, the extent of these processes varies by location and season, depending on factors such as traffic intensity, environmental conditions, and the physiological characteristics of the trees (Soba et al., 2022).

Multiple regression models identified associations between metal concentrations in foliage (surface and absorbed), soil nutrients, and soil pH with growth variables of Fraxinus uhdei (LA, SLA, DW and increase in DBH) (Table 3). These relationships varied across sites and seasons. In the Chapultepec and Tlalpan forests, associations were observed primarily for LA and DW in spring, fall, and winter, and for DBH in summer and winter. This pattern aligns with the seasonal dynamics of tree growth, as leaf expansion occurs in the spring and activity related to radial growth increases in the summer (Varela et al., 2023), whereas in the fall and winter, urban atmospheric conditions promote the accumulation of pollutants due to temperature inversions and lower precipitation, which results in increased deposition of metals on the leaves (Molina & Molina, 2004).

Table 3. Response variables for leaf area (LA), specific leaf area (SLA), diameter at breast height (DBH) and dry leaf weight (DW) by site and season, with significance values (p) and correlation coefficients (Adjusted R²).

LA = Leaf area; SLA = Specific leaf area; DW = Dry leaf weight; DBH = Increase in DBH. CF = Chapultepec Forest; TF = Tlalpan Forest; NP = Naucalli Park.

In the Naucalli Park, these relationships were primarily observed for SLA and increases in DBH in spring and winter, suggesting a seasonal pattern related to resource availability and environmental stress. Within this context, urban trees can serve as a sensitive indicator of the pressures resulting from urban activities (Patel et al., 2023). Overall, the results indicate that the interaction among metals, nutrients, and soil pH helps explain some of the leaf traits and growth of F. uhdei; although its effect depends on environmental conditions and the degree of urban pressure at each site (Omidi et al., 2025).

The leaf area (LA) showed correlations with metal concentrations and soil pH in the Chapultepec and Tlalpan forests (Table 3), with seasonal variations but consistent patterns. In Chapultepec Forest, during the spring, the LA was positively correlated with absorbed copper, surface zinc, and soil pH (indicating that these variables increase the LA) and negatively correlated with surface copper and absorbed zinc (which affect foliage production). In Tlalpan Forest, the LA showed positive correlations with soil pH in fall, and with copper, nickel, and potassium in winter, while chromium, phosphorus and cadmium showed negative correlations. Overall, soil pH and elements such as Cu, Zn, and Ni (which are plant nutrients) showed consistent positive effects, whereas anthropogenic metals such as Cd and Cr were associated with reduced LA. On the other hand, the positive effect of absorbed copper is consistent with its role as an essential nutrient, and surface copper levels may reflect its accumulation, affecting foliar processes (Alcántar-González et al., 2016; Rai, 2016). Furthermore, the positive effect of pH at the study sites suggested that it plays an important role in regulating the availability of nutrients and metals in the soil-plant system (Kabata-Pendias, 2010).

The specific leaf area (SLA) was associated with various elements in the Naucalli Park; in spring, a negative relationship was observed with surface and absorbed chromium and with foliar nitrogen; in winter, surface and absorbed phosphorus showed a negative association. The average chromium concentrations recorded (0.52 mg kg^-1 on the leaf surface and 0.21 mg kg^-1 in the leaf tissue) were lower than those reported in other studies of urban vegetation and are below the levels considered toxic to plants (Kabata-Pendias, 2010; Ramírez-Méndez et al., 2021). However, the negative association between chromium and the SLA suggests that low concentrations of this metal may alter leaf characteristics.

As for nitrogen, the average concentration observed (0.97 %) was below the minimum level generally required for plant growth (≈1.5 %) (Alcántar-González et al., 2016). This condition could lead to an imbalance in the N:P ratio, reducing the capacity for leaf tissue formation and potentially contributing to the decrease in SLA observed in spring and winter. The results indicate that both the presence of metals and the availability of nutrients influence variations in SLA in urban environments, and once again highlight the effects of elements such as chromium, which can affect the structure and function of the leaves.

The diameter at breast height (DBH) was associated with various metals and soil pH at all three sites and across seasons. In Chapultepec Forest, during both summer and winter, both surface and absorbed cadmium were negatively associated with an increase in DBH. In winter, the DBH in Tlalpan Forest was negatively correlated with surface cadmium and lead. For the Naucalli Park in the spring, a negative correlation was observed between the DBH and chromium uptake.

These results suggest that the presence of potentially toxic metals of anthropogenic origin is associated with a lower radial growth rate in F. uhdei, particularly during the winter months when rainfall is reduced. Although the cadmium concentrations recorded in this study remained below the levels considered toxic to plants (3-5 mg kg^-1) (Kabata-Pendias, 2010), this metal can accumulate in plant tissues and affect physiological processes such as transpiration and photosynthesis (Bierza & Bierza, 2024), which may account for its negative association with increased DBH.

The dry weight of leaves (DW) in Chapultepec Forest during the spring was positively correlated with surface zinc and negatively correlated with surface copper and chromium. The beneficial effect of zinc is consistent with its role as an essential nutrient involved in protein stability and plant metabolic processes (Alcántar-González et al., 2016). In contrast, the negative correlation between copper and chromium suggests that their deposition is associated with lower accumulation of leaf biomass.

Vector analyses (Figure 3A-C) revealed negative correlations between the dry weight of 100 leaves and the foliar concentrations of N, P and K suggesting a possible nutrient dilution effect associated with increased leaf biomass. This trend was most evident in K, while N and P showed more moderate changes. The results are consistent with those reported for functional leaf traits, as increases in biomass or changes in leaf structure alter the relative concentration of nutrients without causing nutritional limitations (Binkley et al., 2025). Similarly, the morphological and physiological characteristics of leaves can influence the uptake, retention and accumulation of elements present in the atmosphere.

The results reveal differences among urban sites in the leaf and growth characteristics of Fraxinus uhdei, particularly in the growth of the specific leaf area (SLA) and diameter at breast height (DBH), reflecting variability in the trees’ response under different urban conditions. Both surface and absorbed metals were detected in the foliage, with higher concentrations of Cu and Zn and lower concentrations of Ni, Cr, Cd and Pb; this indicates that the leaves are involved in processes of atmospheric deposition and absorption of elements present in the urban environment.

The regression models revealed associations between metals, nutrients, and soil pH with foliar growth variables (LA, SLA, DW and DBH) ―an indication that the interaction among these factors accounts partly for the variation in tree performance. Overall, the results show that the leaf characteristics and growth of F. uhdei in urban environments are associated with the interaction of metals present in the environment, nutrient availability and soil pH conditions. These findings provide insights into the factors that affect the health and growth of ash trees in urban environments; therefore, they can guide future research and management actions aimed at improving the quality of the urban environment and the resilience of urban vegetation in the face of environmental pressures.

A la administración de los parques Naucalli, Chapultepec y Tlalpan, por las facilidades otorgadas para la colecta de follaje, así como a las autoridades correspondientes por los permisos brindados.

Luz Amelia Sánchez-Landero: experimental and statistical design, drafting of the manuscript and handling of peer reviews; Griselda Benítez-Badillo: data curation; Wendy Sangabriel Conde: formal analysis, revision of the draft; Julio César Pérez Hernández: statistical design, graphs, and review coordination; Gustavo Ortiz Hernández: drafting, statistical analysis; Gerardo Alvarado-Castillo: methodology design; Elio Guarionex Lagunes-Diaz: objectives, methodology design, drafting, and handling of reviews.

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Variable	*Naucalli* *М_е*	*Chapultepec* *М_е*	*Tlalpan* *М_е*	P value
LA	2 065	2 595	2 539	0.140
SLA	56.1^b	66.6^b	78.7^a	0.001
DW	34.90	33.67	29.19	0.105
DBH	1.20^a	0.50^b	0.50^b	0.002

Response variable	Site	Season	Positive predictors	Negative predictores	p-value	**Adjusted R²(%)**
LA	CF	Spring	Absorbed Cu and Cd, surface Zn, and soil pH	Surface Cu and absorbed Zn	0.013	72.7
	CF	Fall	Soil pH	Absorbed Cd and surface Zn	0.002	66.9
	TF	Fall	Surface Ni, Surface and absorbed Cu, and surface K	Surface Cr and P and absorbed Cd	0.011	79.2
SLA	NP	Spring	-------	Absorbed and surface Cr and N	0.003	62.6
SLA	NP	Winter	-------	Surface and absorbed P	0.001	67.1
DBH	CF	Summer	-------	Soil pH and absorbed and surface Cd	0.005	58
	CF	Winter	Absorbed Cr	Absorbed K and Ni; surface Cd	0.001	85.3
	TF	Winter	Absorbed Cr and surface Cu	Surface Cd and Pb; absorbed Cu; surface Ni and N	0.001	99.6
	NP	Spring	-------	Absorbed Cr	0.001	65.5
DW	CF	Spring	Surface Zn	Surface Cu and Cr	0.001	83.8