Urban Forestry & Urban Greening 12 (2013) 69–78
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A study of chemical characteristics of soil in relation to street trees status in Riga (Latvia) Gunta Cekstere ∗ , Anita Osvalde Laboratory of Plant Mineral Nutrition, Institute of Biology of the University of Latvia, 3 Miera Street, LV – 2169, Salaspils, Latvia
a r t i c l e Keywords: Heavy metals NaCl Nutrients Tilia x vulgaris Urban soil
i n f o
a b s t r a c t The chemical composition of soil and appropriate supply of nutrients are very important factors for normal plant growth and development. Lime tree (Tilia x vulgaris H.), is a popular tree species used for urban landscaping in Europe. However, there is little information on the chemical element concentrations available to and recommended for T. x vulgaris in urban soils. The objectives of this study were: (1) to investigate the amount of nutrients, de-icing salts and heavy metals available for uptake by trees in the city centre on a seasonal scale; and (2) to assess the relationship between the vitality of T. x vulgaris and soil chemistry. The research was carried out in five streets and a park in Riga (Latvia) during 2005–2007. Plant-available concentrations of 17 nutrients and heavy metals were determined via 1 M HCl extraction. Soil Cl content, pH, and electrical conductivity were also measured. The investigation revealed a high heterogeneity in soil chemical composition. In total, the element concentrations in urban soils did not exceed values commonly found in urban environments. Higher concentrations of Na, Cl, Ca, Mg, Zn, Cu, and increased pH, but lower P and B concentrations were found in the street soils in comparison to the park soil. Significantly higher concentrations of Na, Cl, and Mg, and lower concentrations of K, Fe, Cu, and B, as well as unfavourable ratios of several element concentrations were found in the soils where more damaged street trees were growing. In addition, the recommended fertilization regimes are discussed. © 2012 Elsevier GmbH. All rights reserved.
Introduction There is a mutual influence between plants and the environment where they are planted and grow. It is difficult to provide a qualitative greenery system in cities due to high building density and traffic volume, as the physiological and visual quality of greenery is influenced by a complex interaction of many environmental factors, e.g., microclimate, soil conditions, air pollution, biotic factors, soil compaction, etc. (Craul, 1999). The chemical composition of soil and appropriate supply with nutrients are very important factors for a normal plant growth and development. There are also differing demands for mineral nutrient content for different plant species (Bergmann, 1988; Rin¸k¸is and Ramane, 1989). In urban areas, various chemical and abrasive materials are used on roads and sidewalks to prevent ice formation during winter. The most common de-icing material used on roads worldwide is sodium chloride (NaCl). Many investigations have demonstrated the harmful effect of Na and Cl on road/street trees (Dobson, 1991; Paludan-Müller et al., 2002; Hartl and Erhart, 2002), e.g.,
∗ Corresponding author. Tel.: +371 29436586; fax: +371 67945417. E-mail addresses:
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[email protected] (G. Cekstere),
[email protected] (A. Osvalde). 1618-8667/$ – see front matter © 2012 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.ufug.2012.09.004
correlations with Tilia spp. leaf and crown damage (Supłat, 1996; Chmielewski, 1996; Chmielewski et al., 1998; Bryson and Barker, 2002; Czerniawska-Kusza et al., 2004; Bach et al., 2006). In trees, the visual symptoms of the damage caused by Na and Cl appear as post-flushing dieback and foliage discoloration, and necrosis of leaves (Leh, 1973; Bryson and Barker, 2002). Another problem is the toxic impact of heavy metals on plants due to heavy metal deposition by transport emissions and other anthropogenic activities (Iqbal and Shafig, 2000; Piczak et al., 2003). Plants require some of these metals (Fe, Mn, Zn, etc.) in trace quantities as essential micronutrients, but they can be phytotoxic at higher concentrations (Alloway, 1995; Kabata-Pendias and Pendias, 2001). The accumulation of heavy metals in urban soils and plants has been studied worldwide (Dyer and Mader, 1986; Linde et al., 2001; Piczak et al., 2003; Madrid et al., 2004; Baycu et al., 2006; Oleksyn et al., 2007). Nevertheless, in a number of studies on heavy metals, sodium, or separate plant nutrients in urban environments, the concentrations of elements in soils are determined as total or “pseudo-total” using aqua regia extraction (Jim, 1998; Yesilonis et al., 2008a; Gałuszka et al., 2011). Such results are not very useful for elucidation of plant mineral nutrition problems, as the majority of the detected element content is not available for plant uptake. The results of different urban soil studies are also
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difficult to compare due to the extreme differences in soil extraction methodologies. The lime tree Tilia x vulgaris H., known also as T. x europea L., T. intermedia DC., T. x hollandica K. Koch, is a popular tree species used for urban landscaping in Central, Northern (Sæbø et al., 2003; Sjöman et al., 2011), and Eastern Europe (Sander et al., 2003). It is also one of the main species of street greenery in Riga, Latvia, which is located in the boreo-nemoral zone. Elimination of street greenery because of tree decline and low vitality has been observed in the ˇ central part of Riga (Cekstere et al., 2005). Unfortunately, there have been few studies and information is scarce on the main factors affecting the vitality of T. x vulgaris in the boreo-nemoral zone. During the 1960s, some investigations about the physical and agrochemical properties of soil and their effect on the growth of physiologically active roots were carried out, as well as some studies on nutrient uptake in and influence on vital¯ ity of lime trees in the street greenery of Riga (Ripa and Petersons, 1968; Ozols et al., 1971). Our first studies on T. x vulgaris, and Aesculus hippocastanum in Riga identified an imbalance in the mineral nutrition of urban trees: decreased concentrations of S, K, Mn were ˇ identified in T. x vulgaris leaves (Cekstere et al., 2005), as well as the toxic effect of NaCl on trees (Cekstere et al., 2008). Research on the species composition of ectomycorrhizal fungi on urban T. x vulgaris trees, showed that it could be affected by elevated amounts of Na and Cu in the soil (Timonen and Kauppinen, 2008). Several studies have analyzed the content of separate chemical elements in T. x vulgaris leaves in relation to leaf damage (Leh, 1973; Kopinga and van den Burg, 1995). Therefore, it is important to explore the soil chemical composition from the tree mineral nutrition aspect, in order to improve the quality of street greenery. The objectives of the research were: (1) to investigate the content of chemical elements (both nutrients, deicing salts, and heavy metals) available for uptake by trees in street and park soils in the city centre on a seasonal scale; and (2) to assess the vitality of Tilia x vulgaris in the study sites in relation to the soil chemical results. Materials and methods Study area The study was conducted in Riga (the capital of Latvia, Eastern Europe), which is situated on the Baltic Sea at the southern part of the Gulf of Riga in the boreo-nemoral zone. The climate in Riga is moderately warm and humid: the average annual precipitation is 700 mm, the average temperature in January is −4.9 ◦ C, but in July +16.9 ◦ C. The average rate of NaCl application in Riga streets is approximately 4.06 kg of salt/m2 (Cekstere et al., 2008). Traffic intensity is increasing in Riga (Anonymous, 2005a). Street greenery currently covers 39% of the overall street length (90 km) of the central part of the city. Soils in the central part of Riga can be characterized as artificial, sandy, highly heterogeneous and compacted. In general, the top-layer of the studied street soils (0–35 cm) contain 8.58 ± 0.44% clay, 13.32 ± 1.26% silt, 78.09 ± 1.57% sand, and organic matter from 3.55 ± 0.29 to 12.27 ± 2.23% (on average 8.00 ± 0.76%), but in Viestura Garden: 10.38 ± 0.0% clay, 24.2 ± 2.7% silt, 65.5 ± 2.7% sand, and 5.70 ± 0.49% organic matter (unpublished data by Cekstere, G.). Field work Soil samples were collected from the beds of 26 street trees with various tree crown condition or vitality, which were located in eight different sites in five streets with intensive traffic in the central part of Riga. Each study site consisted of three to four neighbouring trees
located up to 3 m from the road. Another criterion for the site selection was the type of vehicle traffic as different vehicles produce different types of pollution (Kleperis, 2003; Nikmane et al., 2003). The streets selected for the study were: Hanzas street – heavy traffic consisting of public transport (busses), trucks and motor cars; K. Valdemara street – heavy traffic consisting of public transport (busses and trolleybus), trucks and motor cars; Elizabetes street and Stabu street – medium heavy traffic consisting of motor cars; Basteja blvd. – medium heavy traffic consisting of public transport (trams) and motor cars. The intensity of transport per hour from 8.00 to 18.00 was on average 987 cars in Hanzas street, 800 - in K. Valdemara street, 439 – in Basteja blvd., 280 – in Elizabetes street, 250 – in Stabu street (unpublished data procured from Municipality of Riga Department of Traffic). Soil samples were taken from each roadside street tree bed from 0 to 35 cm depth in March, June and July 2005, and in June and August 2007 (Fig. 1, Table 1). Each soil sample consisted of thoroughly mixed five subsamples (volume of each subsample approximately 0.5 l) collected from each tree bed by a soil probe at a distance of 0.5 to 2 m from the tree trunk. A park – Viestura Garden – in the central part of Riga was chosen in order to assay the city background level or unpolluted area. The soil samples were collected separately from three lime trees at the perimeter area of their crowns. Each soil sample was placed in a plastic bag and immediately transported to the laboratory. Along with the soil sampling, assessment of tree vitality was done to characterize the general physiological status of trees at the end of summer. This was based on the following bioindicators: visual evaluation of crown defoliation (UN/ECE, 1994), and the average intensity of leaf necrosis. Based on the results, the tree condition was classified as healthy (0–10% defoliation, 0% necrosis), slightly damaged (11–25% defoliation, 1–5% necrosis), medium damaged (26–60% defoliation, 6–20% necrosis), and seriously damaged (>61% defoliation, >21% necrosis). Laboratory analysis One of the methods widely used in Latvia to detect the amount of plant available nutrients, is soil extraction with 1 M HCl (Rin¸k¸is and Ramane, 1989). This extraction characterizes not only the amount of element currently available for the plant uptake from the soil, but also indicates the amount of reserves of the element for the remaining vegetation season (Osvalde, 1996). The most important fact – it is possible to detect all the plant nutrients as well as other elements in this extraction, which allows determination of the ratios of element concentrations in soil. Ranges of the optimal element concentrations for this extraction have been determined for the majority of crop species: vegetables, cereals, fruits, etc. (Rinkis and Nollendorf, 1982). Unfortunately, little data are available on the nutrient concentration levels determined by 1 M HCl extraction method for street trees. The soil samples were dried at room temperature, sieved <2 mm and analyzed in the Laboratory of Plant Mineral Nutrition of the Institute of Biology of the University of Latvia immediately after each sampling. The level of K, Ca, Mg, Fe, Mn, Zn, Cu, Na, Cl, as well as soil reaction and electrical conductivity (EC) was measured in the samples collected in 2005 and 2007, but the concentrations of N, P, S, Mo, B, Pb, Cr, Ni, and Cd were analyzed in the samples collected in 2007. To determine the plant-available amounts of macronutrients (N, P, K, Ca, Mg, and S), micronutrients (Fe, Mn, Zn, Cu, Bo, and Mo), Na, Pb, Cd, Cr, and Ni, the soil samples were extracted with 1 M HCl solution, where soil–extractant mixture was 1:5. Cl content and EC were measured by using distilled water extract (soil–distilled water mixture 1:5), but the soil reaction was detected in 1 M KCl (soil–extractant mixture 1:2.5) (Rinkis et al., 1987).
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Table 1 Characterization of the studied sites and status of Tilia x vulgaris in Riga during 2005 and 2007. Site, number of studied trees
Location of trees along the street*
Distance from tree stem to road; size of tree-bed
2. Hanzas street 1; 3 trees 3. Hanzas street 2; 3 4. Elizabetes street; 4
More than 50 m; unrestricted tree-bed Average 2 m; 7.3 m2 Average 2.15 m; 3.7 m2 Average 0.7 m; 9.9 m2
5. K. Valdemara street; 3
Average 0.7 m; 4.2 m2
6. Stabu street 1; 3
0.6 m; 10.0 m2
1. Viestura Garden or park area; 3 trees
2
7. Stabu street 2; 4
Average 0.6 m; 8.8 m
8. Basteja blvd.** 1; 3 9. Basteja blvd.** 2; 3
Average 3.5 m; 25 m2 1.25 m; 8.8 m2
* **
– road; – tree; – pavement; Since 2008 – Z.A. Meierovica blvd.
– street buildings; and
Number and status of trees
28.08.2005
30.08.2007
All healthy
All healthy
All severely damaged All medium damaged 1 – healthy tree, 1 – slightly damaged, 2 – severely damaged 1 – medium damaged, 2 – severely damaged 2 – medium damaged, 1 – severely damaged 1 – slightly damaged, 3 – severely damaged All healthy All severely damaged
All severely damaged All medium damaged 1 – healthy, 3 – severely damaged All medium damaged 2 – medium damaged, 1 – severely damaged 1 – slightly damaged, 1 – medium, 2 – severely damaged All healthy All severely damaged
– parking lot.
The levels of Ca, Mg, Fe, Cu, Zn, and Mn were determined with atomic absorption spectrophotometer (AAS) AAnalyst 700 (PerkinElmer, Singapore), acetylene-air flame, Pb, Cd, Cr, and Ni – on a graphite furnace equipped AAS AAnalyst 700 (Page et al., 1982; Anonymous, 2000). K and Na – with the flame photometer JENWAY PFPJ (Jenway Ltd., Gransmore Green, Felsted Dunmow, Essex, UK). Cl concentrations in the soil samples were determined by the AgNO3 titration method. For P, S and Mo determination, the soil extract was oxidized with HNO3 , H2 O2 and HClO4 , the obtained salts were dissolved in HCl and diluted with distilled water. The levels of N, P, Mo, and B were analyzed by the colorimetry: N – by Nesler’s reagent in an alkaline medium (modified Kjeldal method); P – by ammonium molybdate in an acid reduced medium; Mo – by thiocyanate in reduced acid medium; B – by hinalizarine in sulphuric acid medium; and S – by turbidimetric method by adding BaCl2 with a spectrophotometer JENWAY 6300 (Barloworld Scientific Ltd., Gransmore Green Felstad, Dunmow, Essex, UK). Soil pH – by using the pH-metre Sartorius PB-20 (Sartorius AG, Goettingen, Germany), but EC – with the conductometer Hanna EC 215 (Hanna instruments, USA) (Rinkis et al., 1987).
ecological data. Standard errors (SEs) were calculated in order to reflect the mean results of chemical analysis. The correlation coefficients (Pearson) were classified as follows: r < 0.5 – weak correlation, 0.5 < r < 0.8 – medium correlation and r > 0.8 – high correlation. The Student’s t-test (two-sample assuming equal variances) was used for testing the changes in the chemical element concentrations during 2005 and 2007. To detect differences between the levels of element concentrations in the street greenery soil and the background level (Viestura Garden), as well as between growth environments of damaged and healthy lime trees, a t-test two sample assuming unequal variances was used. Dispersion of chemical element concentrations between research sites was characterized by the variance ( 2 ) parameter. To assess relationships between the element concentrations, soil pH, tree bed properties, age and health status of trees in August 2007 the principal component analysis (PCA) was done using PC-ORD Version 5 (McCune and Mefford, 1999). The chemical parameters for the PCA were selected based on the differences of the chemical results between the healthy and damaged trees, as well as to exclude mutual correlations between the chemical parameters. Results
Statistical analysis The statistical analysis of the research results was done using SPSS 14.0 and PC-ORD software for multivariate analysis of
The study revealed that the majority of T. x vulgaris trees in the centre of Riga in August 2005 and 2007 (Table 1) exhibited signs of damage. In 2007, trees had a higher vitality than in 2005.
Fig. 1. Geographic situation of Latvia (a) and the research sites in Riga Centre (b). Site: 1 – Viestura Garden (background level); 2 – Hanzas street 1; 3 – Hanzas street 2; 4 – ¯ street; 6 – Stabu street 1; 7 – Stabu street 2; 8 – Basteja blvd. 1; and 9 – Basteja blvd. 2. Elizabetes street; 5 – K. Valdemara
August 07
June 2007
July 2005
June 2005
n – number of analyzed soil samples in the research period. SE – standard error. Means with the different letter for the parameter were significantly different (t-test, p < 0.05): the first letter relates to the park level in the same sampling time, the second – to the level of previous sampling time in the same year, the third – to June 2007 in comparison with June 2005.
188.27 ± 13.81ba 96.26–329.06 134.87 ± 9.24bba 71.32–254.75 137.72 ± 11.63bb 58.40–290.29 159.00 ± 9.13aab 98.32–275.68 188.52 ± 15.66ab 58.70–399.60 360.41 ± 17.68aa 326.23–385.38 192.74 ± 19.24aba 162.37–228.40 178.60 ± 8.00ab 165.56–193.16 184.98 ± 30.77aaa 138.05–242.46 176.80 ± 18.43aa 144.30–208.10 724.01 ± 82.26ba 132.25–1568.14 436.57 ± 60.82bba 81.51–1092.44 302.79 ± 50.41bc 47.58–1060.58 275.97 ± 36.89bab 48.81–749.10 204.04 ± 32.60ba 55.62–673.68 29.79 ± 0.69aa 28.59–30.99 27.33 ± 1.94aaa 24.59–31.08 25.36 ± 4.34aa 20.70–34.03 24.36 ± 4.00aaa 17.17–30.98 31.80 ± 5.98aaa 22.4–42.90 129.17 ± 28.45ba 26.16–744.86 65.40 ± 26.52bba 3.40–466.03 27.82 ± 10.21bc 4.71–219.74 41.01 ± 14.69baa 3.68–309.63 40.29 ± 8.81ba 8.71–227.31 5.96 ± 0.42aa 5.13–6.52 5.17 ± 0.38aaa 4.64–5.92 6.46 ± 0.48aa 4.60–6.25 6.76 ± 0.76aaa 5.39–8.02 16.08 ± 4.03ab 10.47–23.89 1.84 ± 0.22ba 0.78–5.33 1.28 ± 0.13bba 0.48–2.93 0.92 ± 0.10bc 0.46–2.29 0.87 ± 0.09bab 0.40–2.05 0.65 ± 0.07bb 0.27–1.57 March 2005
Mean ± SE Range Mean ± SE Range Mean ± SE Range Mean ± SE Range Mean ± SE Range
0.67 ± 0.02aa 0.62–0.69 0.57 ± 0.02aba 0.54–0.60 0.59 ± 0.04aa 0.51–0.66 0.30 ± 0.05aab 0.25–0.39 0.36 ± 0.03aa 0.30–0.40
K
Park (n = 3) Streets (n = 26)
Na
Park (n = 3) Streets (n = 26)
Cl
Park (n = 3) Streets (n = 26)
EC
Park (n = 3)
Sampling time
The results of soil chemical analysis are given in Tables 2–5. In general, they revealed a high heterogeneity or a wide range and variance of element concentrations in the soil. In comparison with the city background level measured in Viestura Garden, increased concentrations of Na and Cl were found in the street soil samples collected near the carriageway, especially at the end of winter 2004/2005, when the average concentration of Na and Cl was, respectively, 24 and 22 times higher than in Viestura Garden. The levels of Ca, Mg, Zn, and Cu, and pH were also higher in the street soil samples, but the concentrations of P, Mn and B were lower than those in the park. The highest concentrations of Cu and Fe (approximately 2–4 times higher than in the park) were found in sites with trolleybus and tram traffic (Sites 5, 8 and 9). A statistically significant tendency for the concentrations of Na, Cl, K, Ca, and Mg to decrease was observed in the street topsoil from March to June 2005. In the summer months, only the concentrations of Na and K were significantly reduced in the street topsoils in 2005, as well as the concentrations of S and Mo in the summer months of 2007 (Tables 2 and 5). Comparing the results of the street soil samples collected in June of 2005 and 2007, significantly higher concentrations of K, Fe, and lower Na concentrations were found in 2007 than in 2005. There was a high positive correlation between the elevated concentrations of Na, Cl and EC in the soil in 2005 and 2007 (max. rCl = 0.89; 06.2005) and a weak positive correlation (p < 0.05) between the studied chemical parameters (min. rCl = 0.40; 03.2005). The concentrations of Ca and Mg in the street soils of Riga showed a medium-high positive correlation with the pH level (max. rMg = 0.76; 06.2005). In addition, a medium-high and high positive correlations were found between the concentrations of Fe and Cu (max. r = 0.84; 08.2007), Fe and Mn (max. r = 0.78; 06.2005), as well as between Ca and Mg (max. r = 0.94; 03., 06.2005), Na and Cl (max. r = 0.73; 08.2007) in the street soils at three and more sampling times. A medium-high positive correlation was determined between the concentrations of Fe and Cr (max. r = 0.76; 08.2007), Cr and Ni (max. r = 0.64; 08.2007), as well as Pb and Zn (max. r = 0.62; 06.2007) in the street soils at both sampling times in 2007. In general, the distribution of the mean element concentrations and concentration ranges in the soil samples clearly revealed the main differences in the growth environment of the lime trees in the park, as well as between healthy and damaged street trees (Table 6). Significantly higher levels of Na, Cl, Mg, and pH, but lower concentrations of K, Fe, Cu, and B were found in soils where more damaged street trees were growing in comparison with the soils where healthy trees were growing. As Cl concentration in the soil samples in summer 2007 was low and highly correlated with Na, but Mg had correlation with pH, and Fe with Cu, these parameters were excluded from the PCA to simplify the data structure (Fig. 2). Therefore the chemical parameters, which were included in the PCA were the results of Na, K, Cu, B, pH in August 2007, when the vitality of trees was also assessed. In general, the PCA results revealed a relatively good structure of the individual sampling points or trees in the ordination space. The first two components explained 59.15% of the total variance. The soil samples of healthy street and park trees were clearly located on the negative side of the Axis 1, but the damaged street trees on the opposite side. The most important factors were K, Na, tree distance from the carriageway, as well as the size of tree bed. Analysis of element ratios (Table 7), which is important factor in plant mineral nutrition, showed that the concentration of Na was about 1.5–2 times lower than the macronutrient K in the soil samples of healthy trees, but for slightly to seriously damaged trees, in general the concentration of K was even four times lower than the Na concentration. Also the Ca:Na and
Streets (n = 26)
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Table 2 Element concentrations (mg/kg) in urban soil samples using 1 M HCl extraction (Na, K) and in distilled water (Cl, EC) in Riga for Tilia x vulgaris during 2005 and 2007.
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Table 3 Element concentrations (mg/kg) in urban soil samples using 1 M HCl extraction in Riga for Tilia x vulgaris during 2005 and 2007. Sampling time
Ca
Mean ± SE Range Mean ± SE Range Mean ± SE Range Mean ± SE Range Mean ± SE Range
March 2005 June 2005 July 2005 June 2007 August 07
Mg
Fe
Park (n = 3)
Streets (n = 26)
Park (n = 3)
Streets (n = 26)
Park (n = 3)
Streets (n = 26)
7408 ± 511aa 6853–8428 6707 ± 1018aaa 4883–8399 6209 ± 808aa 4599–7128 6818 ± 1443aaa 4367–9362 6529 ± 770aa 50,260–7572
16,154 ± 1281ba 6944–27,072 11,008 ± 830bba 2872–16,653 12,203 ± 1009bb 2605–23,671 10,726 ± 795baa 3848–17,442 11,411 ± 912ba 5814–24,758
2088 ± 191aa 1797–2447 2270 ± 361aaa 1740–2960 1796 ± 233aa 1380–2185 2317 ± 455aaa 1472–3031 2488 ± 192aa 2115–2749
5385 ± 500ba 1890–10,269 3711 ± 327bba 644–6817 3965 ± 402bb 471–9279 3702 ± 318baa 1083–7063 3749 ± 345ba 1832–9466
1898 ± 39aa 1823–1958 1429 ± 21aba 1401–1470 1552 ± 93ab 1389–1700 2049 ± 351aaa 1648–2748 2415 ± 94aa 2304–2601
1457 ± 83ba 799–2471 1278 ± 82baa 727–2196 1528 ± 150aa 650–3259 1709 ± 136aab 903–3749 1986 ± 196ba 860–5034
n – number of analyzed soil samples in the research period. SE – standard error. Means with the different letter for the parameter were significantly different (t-test, p < 0.05): the first letter relates to the park level in the same sampling time, the second – to the level of previous sampling time in the same year, the third – to June 2007 in comparision with June 2005.
Table 4 Element concentrations (mg/kg) in urban soil samples using 1 M HCl extraction in Riga for Tilia x vulgaris during 2005 and 2007. Sampling time
Mn
2005 (March + June + July) Mean ± SE Range 2007 (June + August) Mean ± SE Range
Zn
Cu
Park
Streets
Park
Streets
Park
Streets
n=9 243.0 ± 13.7a 151.0–292.1 n=6 329.8 ± 39.8a 219.7–495.6
n = 78 118.8 ± 6.5b 14.9–288.5 n = 52 141.7 ± 9.3b 22.1–288.5
n=9 71.3 ± 7.7a 42.7–108.7 n=6 72.0 ± 10.5a 37.3–104.7
n = 78 110.8 ± 8.8b 24.8–360.7 n = 52 108.9 ± 10.4b 34.2–447.4
n=9 18.0 ± 1.2a 12.4–22.8 n=6 18.9 ± 2.1a 11.3–23.6
n = 78 29.9 ± 2.1b 2.9–92.3 n = 52 30.1 ± 3.5b 3.9–133.2
n – number of analyzed soil samples in the research period (number of trees multiplied by sampling times). SE – standard error. Means with the different letter for the parameter in a row were significantly different from the park level (t-test, p < 0.05).
Table 5 Element concentrations (mg/kg) in urban soil samples using 1 M HCl extraction in Riga for Tilia x vulgaris during summer 2007 (June and August). Element
Park (n = 6)
Street (n = 52)
Mean SE N P S Mo B Pb Cd Cr Ni
38.37 1043.00 16.66 0.04 1.07 63.89 0.20 8.19 1.71
Range ± ± ± ± ± ± ± ± ±
4.94a 167.58a 2.70a 0.00a 0.14a 10.51a 0.02a 0.68a 0.13a
Mean SE
24.05–56.60 535–1598 8.80–26.94 0.03–0.04 0.50–1.51 30.13–93.19 0.15–0.26 6.57–11.29 1.39–2.11
33.14 520.74 15.36 0.04 0.47 51.14 0.20 8.32 1.25
± ± ± ± ± ± ± ± ±
Range 2.04a 27.42b 0.98a 0.00a 0.03b 3.16a 0.01a 0.36a 0.05a
13.97–87.56 253.70–1044.43 7.63–47.94 0.02–0.10 0.07–1.25 18.37–118.27 0.08–0.52 3.25–14.96 0.49–1.97
n – number of analyzed soil samples in the research period (number of trees multiplied by sampling times); SE – standard error; means with the different letter in a row were significantly different from the park level (t-test, p < 0.05).
Table 6 Concentrations of chemical elements (mg/kg) in soil samples in 1 M HCl extraction, Cl and electrical conductivity in distilled water extraction, and soil reaction for Tilia x vulgaris in Riga greenery during 2005–2007. Element
Park
Healthy street trees
Damaged (slightly to seriously) street trees
2005 + 2007 Na Cl K Mg Fe Cu pH/KCl EC (mS/cm) 2007 B
n = 15 27.73 ± 1.64a 7.88 ± 1.31a 218.53 ± 20.49a 2192 ± 132a 1869 ± 114a 18.34 ± 1.08a 6.60 ± 0.06a 0.50 ± 0.04a n=6 1.07 ± 0.14a
n = 20 152.73 ± 21.89b 21.54 ± 6.96b 248.08 ± 17.46a 3014 ± 218b 2123 ± 192a 55.98 ± 6.46b 6.83 ± 0.05b 0.99 ± 0.12b n=8 0.58 ± 0.06b
n = 110 425.21 ± 32.52c 67.86 ± 10.64c 145.97 ± 4.65b 4301 ± 202c 1495 ± 63b 25.70 ± 1.48c 7.04 ± 0.04c 1.13 ± 0.08b n = 44 0.45 ± 0.04c
n – number of analyzed soil samples in the research period (number of trees multiplied by sampling times). Means with the different letter in a row were significantly different (t-test, p < 0.05).
Mg:Na ratio was lower for the damaged street trees in comparison to the healthy trees and trees in the park. An similar average Ca:Mg ratio in the park and street soils was found, but the average Mg:K ratio in the street soils for damaged trees was 2–3 times higher than for healthy street trees, as well as trees in the park. Discussion Chemical characteristics of soil The results of soil chemical analysis revealed several problems and tendencies in the street greenery soils of Riga. Considerably increased concentrations of Na and Cl were found in the street greenery in comparison with the park at the end of winter. The lowest levels of Na and Cl in the soil were found in Site 8 (the healthiest street trees), where the level of pollution in the snow in winter was also low (Cekstere et al., 2008). This research site is located furthest from the carriageway (≈3.5 m), between the pavement and an underground parking lot. This is in a good agreement with other
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Table 7 Mean ratios of element concentrations in 1 M HCl extraction in the street greenery and park soil for Tilia x vulgaris in Riga during 2005–2007. Ratio
Park
Healthy street trees
March 2005; n = 3 Ca/Mg Mg/K K/Na Ca/Na Mg/Na
3.57 5.87 12.14 248.26 69.98
± ± ± ± ±
0.15a 0.82a 0.86a 11.98a 5.38a
Summer 2005 + 2007; n = 12 2.99 12.26 7.01 245.71 82.42
± ± ± ± ±
0.11a 0.89a 0.47a 12.93a 3.78a
March 2005; n = 4 3.72 11.17 1.49 47.63 12.79
± ± ± ± ±
0.26a 2.83b 0.47b 9.58b 2.42b
Damaged (slightly to seriously) street trees Summer 2005 + 2007; n = 16 3.91 14.77 2.25 103.39 26.56
± ± ± ± ±
0.09b 2.16a 0.33b 12.54b 3.24b
March 2005; n = 22 3.08 35.92 0.26 29.83 10.07
± ± ± ± ±
0.11c 4.02c 0.03c 5.25c 1.78b
Summer 2005 + 2007; n = 88 3.03 29.91 0.80 62.45 22.40
± ± ± ± ±
0.06a 1.59c 0.10c 7.58c 2.84b
n – number of analyzed soil samples in the research period (number of trees multiplied by sampling times). Means with the different letter in a row were significantly different in the same research period (t-test, p < 0.05).
studies, which shows that the concentration of Na in soil decreases as the distance from the road increases from 1.5 to 10 m, more rapidly at 5 m distance from the road (Bryson and Barker, 2002). It is estimated that the majority of the applied de-icing material can spread through the air and be deposited within a few metres from the road (Blomqvist and Johansson, 1999; Lundmark and Olofsson, 2007). The decrease in Na and Cl concentrations in the soil in almost all sampling sites during the spring and summer was likely due to leaching from the upper soil layer, percolation deeper into the soil, and uptake by tree roots. That indicates intensive soil pollution with Na and Cl in the street greenery in early spring after the melting of snow and penetration of polluted water into the soil. This could cause stress to plants in spring because plants take up chloride faster than phosphate and sulphate (Bergmann, 1988). Cl anions are also more rapidly leached from the topsoil in comparison with Na in the street greenery soil. Cl usually follows the water flow as a conservative element, which does not participate in chemical reactions, and is not present in soil absorption complexes (Norrström and Bergstedt, 2001; White and Broadley, 2001;
Ramakrishna and Viraraghavan, 2005). However, the level of Na concentration in the soil remained high during the summer, which facilitated regular annual accumulation of this pollutant in the soil. Na can affect the fertility status of the soil by exchanging with the available nutrients in the soil complex, e.g. K+ , NH4 + , Ca2+ , Mg2+ and other cations, and could eventually lead to nutrient deficiencies with subsequent leaching of cations (Dobson, 1991). Furthermore, excess of Na in soil can negatively alter the physical properties of the soil by exchanging with Ca (Davison, 1971; Bryson and Barker, 2002). Therefore, increased soil salinity or EC, especially in spring due to elevated concentrations of Na and Cl, is not favourable for tree mineral nutrition and water regime and can be a reason for “physiological” drought (Dobson, 1991). K is one of the most important antagonistic elements to Na. In the majority of sampling sites, the concentration of K in the street soil was lower than in the park. It was consistent with other studies in urban areas where the soil contained construction and demolition waste (Oleksyn et al., 2007). The obtained K concentrations were in the same level as measured in Riga during 2003–2004
Fig. 2. Distribution of the studied Tilia x vulgaris in Riga within the axes of component analysis for August 2007. (Distance – from tree stem to road; size – P1-P3 – the studied trees in the park; H1–H3 – Hanzas street 1; H4–H6 – Hanzas street 2; E1–E5 – Elizabetes street; K1–K3 – K. Valdemara street; S1–S3 – Stabu street 1; S4–S7 – Stabu street 2; B1–B3 – Basteja blvd. 1; and B4–B6 – Basteja blvd. 2.)
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ˇ (Nollendorfs, 2004, unpublished work; Cekstere et al., 2005), lower than the amount of K measured in roadside soils in Seville, Spain (mean conc. 303 mg/kg, Ruiz-Cortés et al., 2005), but higher than ´ Poland (64–104 mg/kg, Oleksyn et al., 2007). Improved in Poznan, status of K in soil samples was found in 2007. In most of the studied street sites, the level of K was the same as in the park or slightly elevated, and showed a tendency to increase from June to August, probably due to the application of K containing fertilizers. The increased concentrations of Ca and Mg and wide variation of them in the street soil could be connected with the fact that the soils of street greenery in Riga are highly anthropogenic, containing differing amounts of particles and dust of construction materials including bricks, concrete, dolomite chips, etc. In addition to the atmospheric input of alkalizing elements, which have accumulated in the soil heterogeneously and promoted the alkalization of the soil. A similar situation has also been observed in greenery soils in many other cities (Jim, 1998; Craul, 1999; Trowbridge and Bassuk, 2004; Bach et al., 2006; Oleksyn et al., 2007; Pouyat et al., 2007). The level of Mg in Riga was even higher than the total concentrations of Mg in Kielce, Poland (Gałuszka et al., 2011) and Baltimore, USA (Pouyat et al., 2007) which indicated the presence of dolomite chips and dust in the soil. The results on P in soils presented here are consistent with the ¯ studies of Ripa and Petersons (1968) on soils and trees in Riga approximately 40 years ago, where the level of P was high. This could be due to the application of phosphate fertilizers over several decades, and the subsequent formation of hardly soluble P compounds, mainly with Ca and Mg in the neutral and alkaline greenery soils, especially in the park, where the level of P was approximately two times higher than in the street greenery. In general, the concentrations of P in the soils of Riga were the same level as the total P in Kielce (Gałuszka et al., 2011) and Baltimore (Pouyat et al., 2007). In contrast with these findings, Jim (1998) found an insufficiency of P in roadside soils of Hong Kong. Low levels of S and N in the majority of analyzed soil samples were observed in June and August 2007. These results were in a good agreement with studies carried out in other countries (Jim, 1998; Oleksyn et al., 2007; Timonen and Kauppinen, 2008). As anions, S and N are more leachable from soil than cations. This could be a reason for the decrease of S content in the soil during summer. In addition, low levels of S and N in the street greenery soils could be due to the denitrification and gaseous losses of S since the street soils in Riga are very dense. Probably, the mineralization of soil organic matter was not sufficiently intensive to compensate for these losses of N and S. Despite the high demand of plants for N, the supply of N available for uptake is often small and urban soils are commonly perceived to be N deficient (Scharenbroch and Lloyd, 2004). In highly industrialized areas, the requirement of S for plants is often met to a substantial degree by atmospheric SO2 pollution. During the last decades, industrial SO2 emissions have been drastically decreased in Europe (Oulehle et al., 2006), including in Latvia (Jankovska et al., 2008). The established Mo and B concentrations in the street greenery soil in Riga were consistent with the results of the studies carried out in Riga during 2003 and 2004 (Nollendorfs, 2004, unpublished ˇ et al., 2005). They were also within the range of work; Cekstere values found in natural soils in the Riga area (Rin¸k¸is and Ramane, 1989) and in street soils of Poznan´ (Oleksyn et al., 2007). As a soluble anion, B can be easily eluted from soil; therefore, it is seldom available for plant uptake in high concentrations (Rinkis and Nollendorf, 1982). The greenery soil in Riga, both the park and street, can be characterized as abundant with Zn and Cu. In individual soil samples at Sites 2, 4, and 7, the detected concentrations of 1 M HCl extractable Cu in the street soils were close or even exceeded the precautionary limit values of Cu for sandy soils in Latvia – 30 mg/kg (total
75
concentration), while the concentrations of Zn in Riga exceeded the precautionary limit values of Zn for sandy soils in Latvia (250 mg/kg, total concentration) (Anonymous, 2005b). The results for Zn and Cu in Riga street and park soils were almost the same or even higher as the total amount of Zn and Cu in Seville (Madrid et al., 2004) and Baltimore (Yesilonis et al., 2008b), as well as Zn in Hong Kong (Jim, 1998) and Kielce (Gałuszka et al., 2011), indicating that the Zn deposition due to the deterioration of vehicle bodies, common galvanizing of steel surfaces and tire abrasion was more intensive in Riga. The highest concentrations of Cu and Fe found in the streets with trolleybus and tram traffic clearly indicated pollution from electric transport due to abrasion of wires and rails, and the accumulation of dust. Therefore, not only motor (Ozaki et al., 2004), but also electric transport provides a significant input of heavy metal pollution in urban areas. In urban soils, elevated levels of Mn are usually explained by the use of fuel with anti-knock agents containing Mn for motor vehicles (Zayed et al., 1999). The studies in Tallinn, Estonia, have also showed elevated levels of Mn in urban soils in comparison with rural ones (Bityukova et al., 2000). However, our study did not reveal an increased accumulation of Mn in Riga street soils in comparison with the park soils. Wide variation of the amounts of mobile forms of Mn, Fe, Cu, and Zn in 1 M HCl soil extract were found even within one district in Latvia, for instance, in the Riga area – Fe 813–3348, Mn 35–199, Zn 1.5–41.0, and Cu 0.8–6.6 mg/l (Rin¸k¸is and Ramane, 1989) indicating different soil types and usage. The measured Mn and Fe levels in the soil samples of street greenery in the central part of Riga were in the same range of values, but the levels of Zn and Cu could be characterized as elevated. In general, the concentrations of Pb, Cd, Cr, and Ni in the street greenery soil samples were in the same level or even lower as those in the park. The identified heavy metal concentration in the greenery soil samples in the city centre confirmed the research results on Pb and Ni concentrations in roadside soils in 1 M HCl extract in Riga and surroundings presented by Osvalde (1996). It also corresponded to the maximum concentration of Pb (80 mg/kg) allowed by Up¯ıtis and Rin¸k¸is (1992) for plants in soil using 1 M HCl extract. Studies (Linde et al., 2001; Madrid et al., 2004) have shown the highest accumulation of heavy metals in soils close to historical areas and in territories with high road density, as in the city centre. It was not surprising that the concentrations of Pb, Cd, Cr, and Ni in Riga were lower than the total concentrations of heavy metals found in the urban soils of different cities (Jim, 1998; Madrid et al., 2004; Yesilonis et al., 2008b; Liu et al., 2007). It should be stressed that total concentrations of metals are useful for environmental research but hardly suitable for evaluating the phytotoxic impact of heavy metals on street trees. Therefore, the increased concentrations of heavy metals in Riga characterize the general level of plant-available pollution in an urban environment. However, the harmful impact of high concentrations of heavy metals, as well as nutrients on trees in Riga could be softened by the neutral soil reaction and the high content of organic matter. The correlations between the heavy metal concentrations in the street greenery soil indicate a common source of origin for these metals. The positive correlations between the heavy metals in the street soils in Riga correspond to the correlation between Pb and Zn and Cr–Ni found in the street soils in Bucharest (Lacatusu and Lacatusu, 2010), Pb and Zn found in roadside soils in Iran (Saeedi et al., 2009) and Baltimore (Yesilonis et al., 2008b), as well as Fe and Cr in Baltimore (Yesilonis et al., 2008a). In general, the concentrations of all the studied heavy metals and plant micronutrients in the street greenery soil in Riga are ranked in the following order: Fe > Mn ≥ Zn > Pb > Cu > Cr > Ni > Cd. The study revealed that the level of Pb in soils in Riga was higher
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than Cu, mainly due to the intensive use of leaded petrol until the end of 20th century. As a result, Pb could form compounds in the greenery soil, which were not soluble enough to be uptaken by plants or to leach out from the upper soil layer and consequently have a long residence time in urban soils (Brady and Weil, 2002; Yesilonis et al., 2008a). Therefore, in general, the order of the heavy metal concentrations in the soil in Riga corresponds to the order of element concentration in an urban environment (Bityukova et al., 2000; Linde et al., 2001; Madrid et al., 2004; Ruiz-Cortés et al., 2005). Generally, the soils in Riga have sufficient levels of such nutrients as Ca, Mg, P, Fe, Mn, Zn, Cu, and Mo to support lime tree growth, and the levels of Ca, Mg, and Fe are excessive for most plants. Although our data suggest that while the soils in Riga have the potential to be productive for trees, other factors such as high Na, Cl, pH, nutrient imbalance, and tree location close to the carriageway could disturb tree growth. Tree vitality Comparison of soil parameters between the healthy and damaged lime trees revealed several important tendencies. First of all, the PCA results showed a tendency that the soils of healthy limes had increased concentrations of K, and decreased concentrations of Na. The size of the tree-bed and the distance of the tree stem from the carriageway were also important factors, which affected the tree vitality due to less accumulation of de-icing salt. Tree age, Cu, B and pH were less significant factors influencing tree vitality. This indicates that the amount of de-icing salt, which accumulates in each tree-bed during the winter, is a more important factor in Riga. Our findings indicate that by using data of selected parameters, the PCA reflects the factors affecting lime tree vitality relatively clearly. Research results by other scientists have suggested that the soil chemical composition only partially displays the current physiological status of plants (Scharenbroch and Lloyd, 2004), although soil analysis is recommended as a useful method to assess the soil fertility of a growing site or a growing substrate for a new planting of trees (Kopinga and van den Burg, 1995). The results of the present study indicated that 1 M HCl extraction used for the assessment of the plant available content of elements in the urban soil of Riga was useful to reveal disturbances in the tree mineral nutrition and significant differences in the physiological status of trees. The Na concentrations in the street soil of healthy lime trees in Riga were the same as for damaged Tilia cordata L. in Opola, when the salt injury symptoms on leaves appeared at 132 mg/kg Na in soil, but more severe symptoms appeared at 260 mg/kg in September (Czerniawska-Kusza et al., 2004). According to Hootman et al. (1994), 250 mg/kg Na in soil is the threshold to be considered as excessive for most trees. This indicates that T. x vulgaris in Riga is more tolerant than T. cordata to high levels of Na in the soil, however there are also other important factors such as the concentration ratios of antagonistic elements and the level of Na in tree leaves which affect tree vitality. It should be stressed that time of soil sampling (early spring, summer, autumn) could seriously affect the results of chemical analyses of urban soil. This study showed that the most healthy lime trees were found in Site 8, as well as in the park, where on average the highest content of K was found. Our study suggests that the concentration of K in the range from 100 to 200 mg/kg in the soil could be characterized as insufficient for lime trees in conditions of high Na concentrations. Therefore, it is advisable to carry out lime tree fertilization with K fertilizers, if the concentration of K in sandy soil in 1 M HCl extract is less than 200–250 mg/kg, especially during spring. An important factor in the plant mineral nutrition is the K:Na ratio in soil (Dyer and Mader, 1986): if Na > K, disturbances in
nutrient uptake can be found, which have a negative impact on the physiological status of trees (Dobson, 1991). A study in Riga in 2003 and 2004 showed that the optimal K:Na ratio in soil should be at ˇ et al., 2005). In general, the K:Na ratio in the least 2–2.5:1 (Cekstere soil samples from the park and for the healthy street trees during 2005 and 2007 could be characterized as optimal, but for damaged trees – K:Na < 1. Although the K:Na ratio in the soil of both healthy and damaged street trees in Riga ranged widely, and which sometimes fell within the optimal values for trees, the identified low K:Na, as well as the low Ca:Na and Mg:Na ratio in the street soil samples could have an additional harmful impact on tree mineral nutrition. It should be stressed that the most unfavourable element ratios (K:Na, Ca:Na, and Mg:Na) were found at the beginning of the vegetation season, therefore they could have an especially negative impact on tree physiology. While the most favourable Mg and K ratio in soil (1 M HCl extract) for plant mineral nutrition is 2:1 (Rinkis and Nollendorf, 1982), both in the street greenery and in the park soil the Mg:K ratio was higher. Thus, high levels of Mg could probably disturb the K uptake from soil by tree roots. A significant factor affecting plant mineral nutrition is the Ca and Mg ratio (Ca:Mg) in the soil. The most optimal Ca:Mg ratio in soils (1 M HCl extract) for plant nutrition is 5–8:1 (Rinkis and Nollendorf, 1982). The average Ca:Mg ratio found in the street greenery and park soil in Riga was lower, generally 3:1, and therefore unfavourable for Ca uptake from the soil. The neutral and alkaline reaction of anthropogenic soils in urban environments is considered to be one of the main factors responsible for tree growth and ecological status (Fostad and Pedersen, 1997; Jim, 1998; Bach et al., 2006). A pHKCl value above 6.5, which was the most common in Riga, is generally considered as “high” for trees (Kopinga and van den Burg, 1995). Thus high substrate pH can lead not only to lower element availability for plants, but also to depression of microbial activities and mycorrhizal decline (Oleksyn et al., 2007).
Conclusions This study revealed a high heterogeneity in the chemical composition of soil in the centre of Riga even within one street section. In total, the concentrations of studied elements in the greenery soil samples did not exceed the values common in urban areas. However, in the street soils higher concentrations of Na, Cl, Ca, Mg, Zn, Cu, and soil reaction, but lower P and B concentrations were found in comparison with the park soils. Statistically significant tendencies for the concentrations of Na, Cl, K, Ca, and Mg to decrease were observed in the street topsoil from March to June 2005. In the summer, only the concentration of Na, K, S, and Mo were significantly reduced in the street topsoil. In general, the soils in Riga have sufficient levels of Ca, Mg, P, Fe, Mn, Zn, Cu, and Mo to support lime tree growth, and even excessive amounts in the case of Ca, Mg, and Fe for the majority of plants. However, other factors such as high Na, Cl, pH, nutrient imbalance, and proximity of trees to the carriageway could disturb tree growth. The 1 M HCl extraction method used for assessment of the plant available content of elements in the urban soils of Riga was suitable to reveal disturbances in the tree mineral nutrition and significant differences in the physiological status of trees. Significantly higher concentrations of Na, Cl and Mg, lower concentrations of K, Fe, Cu and B, as well as unfavourable ratios of element concentrations (Mg:K, K:Na, Ca:Na, and Mg:Na) were found in soils where more damaged street trees were growing. This was especially pronounced at the beginning of the vegetation season, due to accumulation of de-icing salt in street soils. Thus, reduced use of NaCl as de-icing salt in winter, as well as fertilization with K, if
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the concentration of K in soil is less than 200–250 mg/kg, is recommended to improve the vitality of street trees in the boreo-nemoral zone. In addition, chemical fertilization with N, S and B would be necessary to realize due to low content of these elements in urban soil. Acknowledgments This work was supported by the European Social Fund. The authors thank Professor Olgerts ¸‘ Nikodemus (University of Latvia) and two anonymous reviewers for scientific advises and comments ‘ for in the research accomplishment, as well as Dr. Dainis Run¸gis English corrections of the manuscript. References Alloway, B.J., 1995. Heavy Metals in Soils, 2nd edition. Blackie Academic & Professional, London. Anonymous, 2000. Analytical Methods for Atomic Absorbtion Spectrometry. PerkinElmer Instruments LLC, Singapore. Anonymous, 2005a. R¯ıgas att¯ıst¯ıbas programma 2006–2012.gadam (Riga Development Program 2006–2012, Updated in 2010). Council of Riga, Riga (in Latvian). Retrieved May 2, 2012, from: http://www.likumi.lv/ Anonymous, doc.php?id=120072&from Bach, A., Pawlowska, B., Kraus, D., Malinowska, Z., Pniak, M., Bartyska, M., 2006. Urban ornamental trees reaction to the soil sodium chlorine salinity and pH factor in Krakow. Zeszuty Problemowe Postepow Nauk Rolniczych 510, 39–48 (in Polish). Baycu, G., Tolunay, D., Özden, H., Günebaken, S., 2006. Ecophysiological and seasonal variations in Cd, Pb, Zn, and Ni concentrations in the leaves of urban deciduous trees in Istanbul. Environmental Pollution 143, 545–554. Bergmann, W., 1988. Ernährungsstörungen bei Kulturpflanzen (Nutrient Flow in Crop Plants). Gustav Fischer Verlag, Jena (in German). Bityukova, L., Shogenova, A., Birke, M., 2000. Urban geochemistry: a study of element distributions in the soil of Tallin (Estonia). Environmental Geochemistry and Health 22, 173–193. Blomqvist, G., Johansson, E.L., 1999. Air-borne spreading and deposition of deicing salt – a case study. The Science of the Total Environment 235 (1–3), 161–168. Brady, N.C., Weil, R.R., 2002. The Nature and Properties of Soils, 13th edition. Prentice Hall, Upper Saddle River, New Jersey. Bryson, M.G., Barker, A.V., 2002. Sodium accumulation in soils and plants along Massachusetts roadsides. Communication in Soil Science and Plant Analysis 33 (1–2), 67–78. Cekstere, G., Nikodemus, O., Osvalde, A., 2008. Toxic impact of the de-icing material to street greenery in Riga, Latvia. Urban Forestry and Urban Greening 7, 207–217. Chmielewski, W., 1996. Long-term observations of tree phenology and chemical composition of leaves as indicators of the level of pollution of urban environment. In: Siwecki, R. (Ed.), Biological Reactions of Trees to Industrial Pollution. Sorus, Pozan, pp. 211–218. Chmielewski, W., Dmuchowski, W., Suplat, S., 1998. Impact of urban environmental pollution on growth, leaf damage, and chemical constituents of Warsaw urban trees. In: Bytnerowicz, A., Arbaugh, M.J., Schilling, S.L. (Tech. coords.), Proceedings of the International Symposium on Air Pollution and Climate Change Effects on Forest Ecosystems, Gen. Tech. Rep. PSW-GTR-166, U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, CA, pp. 215–219. Craul, P.J., 1999. Urban Soils. Applications and Practices. John Wiley and Sons, New York. ´ nski, ´ M., 2004. Effect of deicing salts on urban Czerniawska-Kusza, I., Kusza, G., Duzy soils and health status of roadside trees in the Opole region. Environmental Toxicology 19, 296–301. ˇ Cekstere, G., Osvalde, A., Karlsons, A., Nollendorfs, V., Paegle, G., 2005. The effect of urban environment on the mineral nutrition status of street trees in Riga, the problems and possible solution. Acta Universitatis Latviensis, Earth & Environment Sciences 685, 7–20. Davison, A.W., 1971. The effects of de-icing salt on roadside verges. Ecology 8, 555–561. Dobson, M.C., 1991. De-icing Salt Damage to Trees and Shrubs. Forestry Commission Bulletin 101, HMSO, London. Dyer, S.M., Mader, D.L., 1986. Declined urban sugar maples: growth patterns, nutritional status and site factors. Journal of Arboriculture 12, 6–13. Fostad, O., Pedersen, P.A., 1997. Vitality, variation, and causes of decline of trees in Oslo center (Norway). Journal of Arboriculture 23, 155–165. ˛ S., Michalik, A., 2011. Gałuszka, A., Migaszewski, Z.M., Podlaski, R., Dołegowska, The influence of chloride deicers on mineral nutrition and the health status of roadside trees in the city of Kielce, Poland. Environmental Monitoring and Assessment 176, 451–464. Hartl, W., Erhart, E., 2002. Effects of potassium carbonate as an alternative road deicer to sodium chloride on soil chemical properties. Annals of Applied Biology 140, 271–277.
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