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Article

Potential of Selected Species of Spiraea L. for Phytoremediation of Heavy Metals from Soils of Urban Areas

by
Wojciech Antkowiak
1,*,
Maciej Bosiacki
2 and
Mateusz Sowelo
3
1
Department of Botany, Faculty of Agronomy Horticulture and Biotechnology, Poznań University of Life Sciences, Wojska Polskiego 28, 60-637 Poznań, Poland
2
Department of Plant Physiology, Faculty of Agronomy Horticulture and Biotechnology, Poznań University of Life Sciences, Wołyńska 35, 60-637 Poznań, Poland
3
The Botanical Garden, Adam Mickiewicz University Poznań, Wieniawskiego 1, 61-712 Poznań, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(11), 1916; https://doi.org/10.3390/agriculture14111916
Submission received: 26 September 2024 / Revised: 22 October 2024 / Accepted: 26 October 2024 / Published: 29 October 2024
(This article belongs to the Special Issue The Impact of Environmental Factors on the Quality of Horticultural Commodities)
Browse Figure
Versions Notes

Abstract

Four taxa of Spiraea were selected for this study: S. × cinerea Zabel ‘Grefsheim’, S. nipponica Maxim. ‘Snowmound’, S. splendens É. N. Baumann ex K. Koch and S. × vanhouttei (Briot) Carrière growing for a minimum of 5 years along heavily trafficked traffic routes. This study included the genus Spiraea due to its popularity in horticultural practice (commercial availability, widespread in urban environments). In addition, the use of ornamental shrubs for phytoremediation in urban green spaces effectively combines the aesthetic needs of residents with those of caring for the urban environment. This study was conducted in Poznań (population 550,000, the fifth largest city in Poland). Soils and foliage were examined in spring and autumn. Soil pH and specific electrolytic conductivity (EC) were determined. The content of micronutrients (Cu, Fe, Mn, Ni, Zn) and toxic heavy metals (Cd, Cr, Pb) in soil dry matter and leaves was determined. The uptake capacity of bioavailable forms of heavy metals by Spiraea from the soil was analyzed by determining the bioconcentration factor (BCF). It was found that the studied taxa meet the basic requirements for plants used for soil phytoremediation processes, especially for chromium phytoextraction. The degree of salinity of the tested soils did not pose a threat to the shrubs growing there, and most of the sites, despite the alkaline reaction, are suitable for their cultivation. S. × cinerea and S. × vanhouttei have BCFs for lead <1. The remaining taxa are characterized by strong concentrations of all analyzed elements. A particularly high BCF, above 10, was recorded for chromium and high for manganese and nickel.

1. Introduction

The genus Spiraea L. represents deciduous shrubs of the family Rosaceae Juss. There are 80 to 100 species of this genus throughout the world. Spiraea is widespread in the temperate and subtropical zones of the northern hemisphere. The genus has the richest species diversity in the territory of China, with about 70 Spiraea species [1]. The genus Spiraea was included in this study due to its popularity in horticultural practice (commercial availability, prevalence in urban environments). The use of ornamental shrubs for phytoremediation purposes in urban green spaces can effectively combine the aesthetic needs of residents with the needs of caring for the urban environment.
Poznań (52°24′30.0″ N 16°56′03.0″ E; 52.408333, 16.934167) is located in west-central Poland, in the central part of the Greater Poland. It is the fifth largest city in Poland in terms of population (541,316 inhabitants in 2023) and ninth in terms of area (261.9 km2). In total, public roads in Poznań in 2021 were 1073 km long. The city’s green areas cover an area of 70 km2, i.e., 27% of the entire city area. The city is an important road and railway junction, and the Poznań-Ławica international airport also operates here. Poznań is a center of industry, trade, logistics and tourism. The food industry, production of machines and electrical equipment, motor vehicles, chemicals and rubber products dominate. Poznań is also a large production, service, transport and trade center. Poznań is dominated by sandy and clay-sandy soils. They also encountered Tertiary clays of the Poznań facies (Poznań clays). Urban soils in which the tested plants grew are exposed to heavy metal contamination. Their main source is substances produced during the abrasion of car tires, abrasion of road surfaces and fuel combustion.
Heavy metal contamination of urban soils is an issue that has been studied in research centers around the world [2,3,4,5,6,7,8]. The term heavy metals is usually defined as elements with a minimum density of 4.5 g cm−3, although some consider values in the range of 3.5 to 7 g cm−3 as the lower limit [9]. This group includes both micronutrients (Cu 8.95 g cm−3, Fe 7.87 g cm−3, Mn 7.47 g cm−3, Ni 8.91 g cm−3, Zn 7.14 g cm−3) and toxic heavy metals such as Cd (8.65 g cm−3), Cr (7.17 g cm−3) and Pb (11.34 g cm−3). High concentrations of micronutrients in the soil are harmful—they may even be toxic to plants.
The average content of selected heavy metals in the 0–20 cm layer of agricultural soils in Poland is Pb—13.7 mg kg−1, Cd—0.22 mg kg−1, Ni—6.3 mg kg−1, Zn—32.5 mg kg−1, Cu—6.5 mg kg−1 [10]. In turn, the average content of selected elements for the humus layer of European soils is Pb—15 mg kg−1, Cd—0.145 mg kg−1, Ni—14 mg kg−1, Zn—48 mg kg−1 and Cu—12 mg kg−1 [11]. These values for urbanized areas may present themselves differently, depending on the type and degree of industrialization in present or historical terms. Typically, the presence of heavy metals on urban sites is mainly of anthropogenic rather than lithogenic origin [12,13]. This is related to, among other things, exhaust emissions, widespread industrialization and low-level emissions [14,15,16]. According to Bosiacki [17], the permissible standard for the content of Cd, Cr, Ni and Pb in soils in green areas located near routes in Poznań was not exceeded. The authors found that the content was Cd 0.16–0.42, Cr 0.26–0.67, Ni 0.43–1.25 and Pb 0.79–42.96 mg kg−1 d.m. The authors also found that in the vicinity of selected communication routes in the city of Poznań, most of the tested soils had an alkaline reaction pH > 7.4, which may significantly affect the habitat conditions of plants.
Some heavy metals, although counted as nutrients, can be excessively taken up by plants from overly abundant growing sites and have a detrimental effect on them. An example is iron, which is 80% present in photosynthesizing tissues, but an excess of it leads to the overproduction of reactive oxygen species, affecting the formation of oxidative stress and resulting in the disruption of basic plant metabolism [18,19]. Elements such as mercury, cadmium and chromium are characterized by toxic effects affecting reduced growth and biomass accumulation, disruption of gas exchange, photosynthesis and the mechanism of water and nutrient uptake [20,21,22,23]. In addition, heavy metals also have toxic effects on soil microorganisms, with the following degrees of toxicity being the most common: Cd > Cu > Zn > Pb [24]. This is an important aspect, as microorganisms determine the fertility and biological productivity of the soil, which consequently translates into the yield of crops grown [25]. Although the soils of roadside areas and road separation strips are not used for food production, it is beneficial from the point of view of growing ornamental plants to have as much microbial activity as possible. Ensuring optimal plant growth conditions determines the success of growing both ornamental [26] and utility crops. In the case of land intended for landscaping characterized by excessive heavy metal content, phytoremediation can be a process preceding the target crop [27]. For this purpose, plants that store large amounts of elements in their aboveground parts (hyperaccumulators) or plants that deposit smaller amounts of elements but produce a large biomass of aboveground parts are used [28]. In addition to heavy metals, high salinity is also a problem, which also contributes to inhibiting the growth of cultivated plants [29].
The bioconcentration factor (BCF) is used to assess the degree of heavy metal accumulation in plants. It is the quotient of the concentration of metals in plant tissues (mg kg−1) to the concentration of metals in soil (mg kg−1) [30,31,32]. Depending on the nature of the study, this method is used to determine the concentration of heavy metals in roots, in shoots or only in selected organs [33,34,35,36]. In addition, the BCF coefficient, based on the plant’s ability to extract heavy metals from the soil, makes it possible to compare individual taxa against each other in terms of phytoremediation potential [35]. With few exceptions, most plants have a bioconcentration factor for heavy metals and semi-metals of less than 1 [37]. Plant-growing sites in the city may not only be characterized by a significant content of heavy metals in the soil but also by high salinity. Particularly vulnerable to this factor are plants growing on roadside sites, into which sodium chloride and, in 2% of cases, calcium chloride or magnesium chloride used for de-icing pavement penetrate [38], with NaCl showing greater toxicity to plants than CaCl2 [39]. Studies have proven a correlation between sodium and chlorine content in the soil, and increased sodium and chlorine accumulation in plants affects the reduction of biomass, the occurrence of chlorosis and necrosis on leaves, and, in extreme cases, also leads to the death of entire plants [29,39,40,41,42,43]. According to Equiza et al. [44], significant post-winter soil salinity levels in roadside sites can persist for almost the entire growing season. Soil alkalinization due to the use of de-icing agents is also an important aspect [45,46]. To date, only a few spirea taxa (S. × cinerea ‘Grefsheim’, S. betulifolia, S. japonica, S. media, S. nipponica and S. thunbergii) have been included in studies to test their resistance to salinity [47,48].
The aim of the research was to determine the potential of the species Spiraea growing in urbanized areas for phytoremediation of heavy metals based on the content of micronutrients (Cu, Fe, Mn, Ni, Zn) and toxic metals (Cd, Cr, Pb) in the leaves and soil of their cultivation sites, as well as the bioconcentration factor. The soils of the cultivation sites in Poznań, Lublin, and Gdańsk were also analyzed for pH and specific electrical conductivity to expand knowledge about the cultivation conditions of these plants in major urban centers in Poland.

2. Materials and Methods

For this study, four taxa of Spiraea L. were selected: S. × cinerea ‘Grefsheim’, S. nipponica ‘Snowmound’, S. splendens (=S. densiflora) and S. × vanhouttei growing for a minimum of 5 years on three sites located directly on traffic routes with heavy traffic. In most cases, these plants were at least a dozen years old. Two medium samples were taken from each location of Poznań. Each consisted of 25 individual soil samples taken with an Egner stick from a depth of 0–20 cm. Two samples of fresh leaves were also collected from each site. Each sample consisted of leaves collected from 15 drawn shrubs. Leaves and soil were collected in spring (second half of May) and autumn (second half of September). The criteria for selecting sites from Gdańsk and Lublin and the sampling methods were the same as those for Poznań. GPS coordinates of the sampling sites are included in Tables 4 and 5.
All soil samples were dried, sieved and cleaned of mechanical impurities. Soil pH (pH in H2O) was analyzed using the potentiometric method, and specific electrical conductivity (EC; mS cm−1) was analyzed using the conductometric method. Both tests were carried out on an aqueous extract basis with a soil dry weight to water volume ratio of 1:2 (v/v). Available heavy metals, including micronutrients (Cu, Fe, Mn, Ni, Zn) and toxic heavy metals (Cd, Cr, Pb), were extracted from soil dry weight using a modified Lindsay solution [49], in which pentetic acid (DTPA) was replaced with ethylene-descorbic acid (EDTA). The composition of the solution—5 g of EDTA, 9 cm3 of 25% NH4OH solution, 4 g of citric acid and 2 g of Ca(CH3COO)2 2H2O in 1 dm3—was adopted from Bosiacki et al. [27]. The content of micronutrients and heavy metals was determined by flame atomic absorption spectroscopy (FAAS) with an AAS-5 spectrophotometer (Carl Zeiss, Jena, Germany).
The leaves were dried in an extractor dryer at 105 °C for 48 h and mineralized in a mixture of HNO3 and HClO4 acids (3:1 v/v). The contents of Cu, Fe, Mn, Ni, Zn, Cd, Cr and Pb were determined using flame atomic absorption spectroscopy (FAAS) with an AAS-5 spectrophotometer (Carl Zeiss, Jena, Germany).
The studied spirea were analyzed for their ability to take up bioavailable forms of heavy metals from the soil. For this purpose, the bioconcentration factor BCF was determined. In order to interpret the results obtained, it was assumed, following Lugwisha and Othman [28,29], that a BCF above 1 indicates strong uptake of a given metal from the soil and its concentration in the organs studied. On the other hand, a result below 1 indicates weak or, in the case of a value close to 0, negligible uptake and concentration. The coefficient was calculated based on average values. BCF was calculated as follows:
B i o c o n c e n t r a t i o n   F a c t o r B C F = M e t a l   c o n c e n t r a t i o n   i n   p l a n t   l e a v e s   ( m g   k g − 1 d . m . ) M e t a l   c o n c e n t r a t i o n   i n   s o i l   ( m g   k g − 1 d . m . )

3. Results

The copper content of the soils in which S. splendens was grown ranged from 0.63 to 5.53 mg kg−1 d.m. and had strong variability (57.14% CV) (Table 1). In soils in which S. nipponica ‘Snowmound’ was grown, there was strong variability in copper content (62.76% CV), and the content of this metal ranged from 0.56 to 4.43 mg kg−1 d.m. (Table 1). The copper content in soils in which S. × vanhouttei was grown ranged from 2.54 to 6.08 mg kg−1 d.m. and had low variability (23.83% CV) (Table 1). In the soils in which S. × cinerea ‘Grefsheim’ was grown, there was strong variability in copper content (46.28% CV), and the content of this metal ranged from 1.82 to 6.21 mg kg−1 d.m. (Table 1). Regardless of the date of soil sampling, the highest average copper content was found in soils in which S. × vanhouttei was grown, while the lowest was found in soils in which S. nipponica ‘Snowmound’ was grown (Table 2).
Copper content in leaves of S. splendens ranged from 3.04 to 11.45 mg kg−1 d.m. and had an average variability of 44.18% CV (Table 1). There was a low variability of copper content of 21.57% CV in the leaves of S. nipponica ‘Snowmound’, and the content of this metal in the leaves ranged from 3.95 to 7.04 mg kg−1 d.m. (Table 1). The copper content in the leaves of S. × vanhouttei ranged from 3.34 to 7.93 mg kg−1 d.m. and had an average variability (29.48% CV) (Table 1). Leaves of S. × cinerea ‘Grefsheim’ also showed average variability in copper content (39.78% CV), and the content of this metal ranged from 4.67 to 14.42 mg kg−1 d.m. (Table 1). The highest copper content in leaves was found in S. × cinerea ‘Grefsheim’ (Table 3).
Iron content in the soils in which S. splendens was grown ranged from 25.45 to 88.51 mg kg−1 d.m. and had an average variability (41.30% CV) (Table 1). In soils in which S. nipponica ‘Snowmound’ was grown, there was low variability in iron content (15.90% CV), and the content of this metal ranged from 43.40 to 70.11 mg kg−1 d.m. (Table 1). Iron content in soils in which S. × vanhouttei was grown ranged from 38.70 to 90.10 mg kg−1 d.m. and had average variability (30.87% CV) (Table 1). In soils in which S. × cinerea ‘Grefsheim’ was grown, there was low variability in iron content (21.41% CV), and the content of this metal ranged from 39.26 to 79.10 mg kg−1 d.m. (Table 1). Regardless of the date of collection of soil samples, there were no significant differences in the iron content of the soils in which the studied spirea was grown (Table 2).
Iron content in leaves of S. splendens ranged from 218.27 to 507.75 mg kg−1 d.m. and had an average variability of 27.77% CV (Table 1). There was a low variability of 21.61% CV in the iron content of S. nipponica ‘Snowmound’ leaves, and the content of this metal in leaves ranged from 194.36 to 378.46 mg kg−1 d.m. (Table 1). Iron content in leaves of S. × vanhouttei ranged from 195.99 to 398.18 mg kg−1 d.m. and had a low variability (22.77% CV) (Table 1). The leaves of S. × cinerea ‘Grefsheim’ also showed low variability in iron content (22.33% CV), and the content of this metal ranged from 284.07 to 541.13 mg kg−1 d.m. (Table 1). The lowest iron content was obtained in the leaves of S. nipponica ‘Snowmound’ and S. × vanhouttei (Table 3), while the highest iron content was found in the leaves of S. × cinerea ‘Grefsheim’.
The content of manganese in soils in which S. splendens was grown ranged from 2.97 to 11.11 mg kg−1 d.m. and was characterized by strong variability (49.13% CV) (Table 1). In soils in which S. nipponica ‘Snowmound’ was grown, there was low variability in manganese content (19.82% CV), and the content of this metal ranged from 3.83 to 7.85 mg kg−1 d.m. (Table 1). The content of manganese in soils in which S. × vanhouttei was grown ranged from 2.78 to 12.43 mg kg−1 d.m. and had a strong variability (56.67% CV) (Table 1). The soils in which S. × cinerea ‘Grefsheim’ was grown showed average variability in manganese content (33.49% CV), and the content of this metal ranged from 3.46 to 9.32 mg kg−1 d.m. (Table 1). There were no significant differences in the average manganese content of the soils in which the studied spirea was grown (Table 2).
The manganese content of S. splendens leaves ranged from 35.90 to 109.32 mg kg−1 d.m. and had an average variability of 38.35% CV (Table 1). There was a low variability of manganese content of 14.03% CV in the leaves of S. nipponica ‘Snowmound’, and the content of this metal in the leaves ranged from 31.43 to 48.61 mg kg−1 d.m. (Table 1). The manganese content in the leaves of S. × vanhouttei ranged from 47.48 to 111.00 mg kg−1 d.m. and had an average variability (27.35% CV) (Table 1). Leaves of S. × cinerea ‘Grefsheim’ also showed average variability in manganese content (38.99% CV), and the content of this metal ranged from 31.00 to 98.64 mg kg−1 d.m. (Table 1). The lowest manganese content was obtained in leaves of S. nipponica ‘Snowmound’ (Table 3), while the highest content was found in leaves of S. × vanhouttei.
The nickel content of the soils in which S. splendens was grown ranged from 0.03 to 0.24 mg kg−1 d.m. and was characterized by strong variability (50.00% CV) (Table 1). The soils in which S. nipponica ‘Snowmound’ was grown also showed strong variability in nickel content (66.67% CV), and the content of this metal ranged from 0.01 to 0.21 mg kg−1 d.m. (Table 1). The nickel content in soils in which S. × vanhouttei was grown ranged from 0.07 to 0.33 mg kg−1 d.m. and had strong variability (47.37% CV) (Table 1). The soils in which S. × cinerea ‘Grefsheim’ was grown showed average variability in nickel content (40.00% CV), and the content of this metal ranged from 0.09 to 0.28 mg kg−1 d.m. (Table 1). The highest nickel content was found in soils in which S. × vanhouttei was grown, while the lowest content was found in soils in which S. nipponica ‘Snowmound’ was grown (Table 2).
The nickel content of S. splendens leaves ranged from 0.74 to 1.92 mg kg−1 d.m. and had an average variability of 31.06% CV (Table 1). There was a low variability of 19.15% CV in the nickel content of S. nipponica ‘Snowmound’ leaves, and the content of this metal in leaves ranged from 0.64 to 1.15 mg kg−1 d.m. (Table 1). The nickel content in S. × vanhouttei leaves ranged from 0.94 to 1.58 mg kg−1 d.m. and had a low variability (16.41% CV) (Table 1). The leaves of S. × cinerea ‘Grefsheim’ showed low variability in nickel content (20.12% CV), and the content of this metal ranged from 1.18 to 2.13 mg kg−1 d.m. (Table 1). The lowest nickel content was obtained in the leaves of S. nipponica ‘Snowmound’ (Table 3), while the highest content was found in the leaves of S. × cinerea ‘Grefsheim’.
Zinc content in soils in which S. splendens was grown ranged from 7.10 to 16.02 mg kg−1 d.m. and had average variability (30.68% CV) (Table 1). The soils in which S. nipponica ‘Snowmound’ was grown also showed average variability in zinc content (33.66% CV), and the content of this metal ranged from 3.56 to 13.65 mg kg−1 d.m. (Table 1). Zinc content in soils in which S. × vanhouttei was grown ranged from 8.13 to 23.45 mg kg−1 d.m. and had an average variability (33.47% Cv) (Table 1). The soils in which S. × cinerea ‘Grefsheim’ was grown showed average variability in nickel content (34.65% CV), and the content of this metal ranged from 4.78 to 18.23 mg kg−1 d.m. (Table 1). The highest zinc content was found in soils where S. × vanhouttei was grown (Table 2).
The zinc content in the leaves of S. splendens ranged from 19.63 to 30.11 mg kg−1 d.m. and had a low variability of 13.36% CV (Table 1). There was a low variability of 5.35% CV in the zinc content of the leaves of S. nipponica ‘Snowmound’, and the content of this metal in the leaves ranged from 16.46 to 19.56 mg kg−1 d.m. (Table 1). The zinc content in the leaves of S. × vanhouttei ranged from 31.29 to 50.10 mg kg−1 d.m. and had a low variability (16.41% CV) (Table 1). Leaves of S. × cinerea ‘Grefsheim’ showed average variability in zinc content (34.90% CV), and the content of this metal ranged from 33.70 to 92.04 mg kg−1 d.m. (Table 1). The lowest zinc content was obtained in the leaves of S. nipponica ‘Snowmound’ and S. splendens (Table 3), while its highest content was found in the leaves of S. × cinerea ‘Grefsheim’.
The cadmium content in the soils in which S. splendens was grown ranged from 0.11 to 0.30 mg kg−1 d.m. and had average variability (38.89% CV) (Table 1). In soils in which S. nipponica ‘Snowmound’ was grown, there was low variability in cadmium content (21.74% CV), and the content of this metal ranged from 0.16 to 0.32 mg kg−1 d.m. (Table 1). Cadmium content in soils in which S. × vanhouttei was grown ranged from 0.10 to 0.34 mg kg−1 d.m. and had average variability (36.36% CV) (Table 1). In soils in which S. × cinerea ‘Grefsheim’ was grown, there was strong variability in cadmium content (95.24% CV), and the content of this metal ranged from 0.07 to 0.80 mg kg−1 d.m. (Table 1). There were no statistically significant differences in the cadmium content of the soils between the sites where the spirea was grown, and there was no effect of the date of soil sampling on the density of this metal in the soils (Table 2).
Cadmium content in S. splendens leaves ranged from 0.83 to 1.82 mg kg-1 d.m. and had an average variability of 27.41% CV (Table 1). There was a low variability of 23.70% CV in the cadmium content of S. nipponica ‘Snowmound’ leaves, and the content of this metal in the leaves ranged from 0.94 to 1.75 mg kg−1 d.m. (Table 1). The cadmium content in S. × vanhouttei leaves ranged from 0.75 to 1.61 mg kg−1 d.m. and had an average variability (36.36% CV) (Table 1). Leaves of S. × cinerea ‘Grefsheim’ showed average variability in cadmium content (28.91% CV), and the content of this metal ranged from 0.83 to 1.98 mg kg−1 d.m. (Table 1). There were no statistically significant differences in the cadmium content of soils between sites where spirea was grown, and there was no effect of the date of soil sampling on the density of this metal in soils. The lowest cadmium content was found in the leaves of S. × vanhouttei (Table 3). The other spirea were characterized by significantly higher amounts of cadmium in their leaves.
The chromium content in the soils in which S. splendens was grown ranged from 0.18 to 1.64 mg kg−1 d.m. and had strong variability (65.33% CV) (Table 1). There was also strong variability in chromium content (92.86% CV) in soils in which S. nipponica ‘Snowmound’ was grown, and the content of this metal ranged from 0.01 to 2.67 mg kg−1 d.m. (Table 1). The chromium content in soils in which S. × vanhouttei was grown ranged from 0.28 to 0.97 mg kg−1 d.m. and had an average variability (41.27% CV) (Table 1). In soils in which S. × cinerea ‘Grefsheim’ was grown, there was a strong variability in chromium content (68.13% CV), and the content of this metal ranged from 0.15 to 1.96 mg kg−1 d.m. (Table 1). The highest chromium content was found in soils in which S. nipponica ‘Snowmound’ was grown, while the lowest was found in soils in which S. × vanhouttei was grown (Table 2).
The chromium content of S. splendens leaves ranged from 5.80 to 16.70 mg kg−1 d.m. and had an average variability of 37.73% CV (Table 1). There was an average variation of 35.06% CV in the chromium content of S. nipponica ‘Snowmound’ leaves, and the content of this metal in the leaves ranged from 6.43 to 18.81 mg kg−1 d.m. (Table 1). The chromium content in S. × vanhouttei leaves ranged from 4.29 to 12.79 mg kg-1 d.m. and had an average variation (36.69% CV) (Table 1). Leaves of S. × cinerea ‘Grefsheim’ showed average variability in cadmium content (35.29% CV), and the content of this metal ranged from 7.02 to 19.61 mg kg−1 d.m. (Table 1). The lowest chromium content was obtained in the leaves of S. × vanhouttei (Table 3), while significantly higher contents of this metal were found in the leaves of the other spirea.
Soils in which S. × cinerea ‘Grefsheim’ was grown showed strong variability in lead content (71.52% CV), and the content of this metal ranged from 1.25 to 9.45 mg kg−1 d.m. (Table 1). The content of lead in soils in which S. splendens was grown ranged from 1.11 to 4.57 mg kg−1 d.m. and was characterized by strong variability (52.42% CV). Soils in which S. nipponica ‘Snowmound’ was grown showed average variability in lead content (42.15% CV), and the content of this metal ranged from 1.03 to 3.90 mg kg−1 d.m. Lead content in soils in which S. × vanhouttei was grown ranged from 0.64 to 12.85 mg kg−1 d.m. and was characterized by strong variability (62.54% CV). Regardless of the date of collection of soil samples, the lowest average lead content was found in soils in which S. nipponica ‘Snowmound’ (2.23 mg kg−1 d.m.) and S. splendens (2.27 mg kg−1 d.m.) was grown, while the highest was found in soils in which S. × vanhouttei was grown (6.94 mg kg−1 d.m.) (Table 1). There was no effect of the harvest date of the soil samples on the content of this metal in the soils in which the spirea was grown.
Lead content in the leaves of S. × cinerea ‘Grefsheim’ ranged from 2.60 to 4.73 mg kg−1 d.m. (Table 1). As in the case of the other spirea, there was low variability in lead content (21.39% CV). In the leaves of S. splendens, the lead content ranged from 2.71 to 4.86 mg kg−1 d.m., in S. nipponica ‘Snowmound’ from 3.00 to 4.90 mg kg−1 d.m., in the leaves of S. × vanhouttei it ranged from 2.69 to 3.83 mg kg−1 d.m. Regardless of the date of harvesting the soil samples, the lowest average lead content was found in the leaves of S. × vanhouttei (3.16 mg kg−1 d.m.). The other spirea were characterized by significantly higher leaf lead content (Table 1).
The timing of the collection of leaves for analysis had a significant effect on their heavy metal content. Significantly higher contents of lead, cadmium, chromium, nickel, zinc, iron and manganese, regardless of the taxon of the spirea, were found in leaves harvested in spring compared with the content found in leaves harvested in autumn. In the case of copper, no significant differences were found in the content of this metal in leaves depending on their harvest date (Table 3).
The values of bioconcentration factors for micronutrients and toxic heavy metals are shown in Figure 1. Only S. × cinerea ‘Grefsheim’ and S. × vanhouttei have a BCF for lead < 1. The remaining spirea are characterized by strong concentrations of all analyzed elements. A particularly high bioconcentration factor, above 10, was recorded for chromium and high for manganese and nickel.
The results of soil reaction and specific electrical conductivity for Poznań are summarized in Table 4; those obtained for Lublin and Gdańsk are shown in Table 5.
Both the smallest and the largest soil reaction in Poznań are characterized by the sites of S. × vanhouttei (pH 6.9–8.5); S. nipponica ‘Snowmound’ was planted in sites with the highest soil reaction (pH 7.70–7.95). The specific electrical conductivity of soil samples analyzed in spring is noticeably higher than that of those tested in autumn. Particularly noticeably higher total salt concentrations can be seen in the soils of Garbary Street (with S. splendens growing there) and Żeromskiego Street (S. × cinerea ‘Grefsheim’). In Lublin, S. splendens has particularly unfavorable living conditions, growing at Nadbystrzycka in soil with a pH of 7.90, and S. × cinerea ‘Grefsheim’ from aleja Wincentego Witosa, in soil with an electrical conductivity of 0.258 mS cm−1. In Gdańsk, the highest soil reaction was found at the Aleja Rzeczypospolitej traffic circle (pH H2O—8.19). On the Wały Jagiellońskie, S. × vanhouttei grew in soil that showed an electrical conductivity of 0.471 mS cm−1 during the summer.

4. Discussion

From the point of view of caring for the urban environment, street greenery can provide a remedy for the lingering toxic metals in the soil. One of the methods used in the process of soil phytoremediation is the phytoextraction of elements with the help of aboveground parts of plants [17]. The effectiveness of phytoextraction is determined by two key factors: high biomass production and a bioconcentration factor higher than 1 [37]. It is difficult to estimate the biomass of the spirea differing in growth vigor and habit, but it is worth noting that many of the recognized hyperaccumulators are herbaceous plants reaching small sizes, such as Thlaspi caerulescens, Arabidopsis halleri, Elsholtzia splendens and Viola baoshanensis [50]. Against their background, the biomass production of the studied taxa of the spirea does not fare badly, and their bioconcentration coefficient is high, especially for chromium; however, such a state of bioaccumulation was found at a low content of heavy metals in the soil. The extraction of elements is strong, and the studied shrubs are promising for use in soil remediation processes, but there is not enough data to show the spirea as hyperaccumulators, especially since a taxon, in order to be classified as a hyperaccumulator and be included in the Global Hyperaccumulator Database, should contain in dry leaf mass >100 mg kg−1 of cadmium, thallium or selenium, >300 mg kg−1 of cobalt, copper or chromium, >1000 mg kg−1 of nickel, arsenic, lead or rare earth elements, >3000 mg kg−1 of zinc or >10,000 mg kg−1 of manganese under growth conditions in its natural environment [51]. The phrase “natural environment” may seem problematic for plants that are cultivars, such as S. × vanhouttei and S. × cinerea ‘Grefsheim’. In addition, plants that are facultative hyperaccumulators may take up small amounts of heavy metals at their natural sites, as they are poor in them, while relocated to heavily contaminated areas may show significant remediation potential.
According to Ciążela and Siepak [52], soils adjacent to Poznań exit roads, within 5 m from the roadway in its near-surface layer, have the highest content of Pb, Cd, Cr, Ni, Zn and Cu. The factor that increases the migration of heavy metals is the wind; hence, this distance can increase with its direction. It is also worth mentioning that the metals that most often contaminate the soils of Poznań are zinc, lead and copper [53]. In the case of lead, only S. splendens and S. nipponica ‘Snowmound’ show strong bioconcentration with a BCF value of 1.75 each. In contrast, S. × cinerea ‘Grefsheim’ and S. × vanhouttei accumulate lead weakly in their leaves, with BCFs of 0.86 and 0.46, respectively. Meanwhile, the bioconcentration factor for zinc and copper of all spirea tested is above 1, with the highest BCF = 4.7 for zinc in S. × cinerea ‘Grefsheim’ and BCF = 2.65 for copper in S. splendens.
Using ornamental shrubs to remediate urban soils can be both practical and aesthetically pleasing. The fact is that shrub pruning treatments are commonly used in green spaces regardless of whether or not we use them to extract heavy metals from the soil. Thus, it is possible to combine attention to the decorative aspect of cultivated plants, which is associated with their maintenance pruning, with a deliberate process of phytoremediation. For example, S. splendens blooms at the top of this year’s long shoots, and spring pruning of its shoots is carried out annually. As a result of the treatment, the plant develops numerous shoots of offshoots, which translates into more abundant flowering. It is possible to deliberately change the timing of pruning from spring to autumn before the onset of leaf fall. Phenological observations have determined the onset of leaf fall in S. splendens in late October or early November. However, a considerable part of the dead leaves remain on the stems until about mid-February. Such developmental peculiarities of the spirea allow it to be pruned in mid-October, during the period when the plant gradually enters dormancy, resulting in a negligible risk of activating dormant buds. Autumn pruning, on the other hand, makes it possible to remove shoots with extracted heavy metals from the growing site, and it is worth noting that such treatment will translate into more abundant flowering in the following growing season. In the case of S. × vanhouttei and S. nipponica ‘Snowmound’, inflorescences develop on short lateral shoots growing along last year’s long shoots, while in S. × cinerea ‘Grefsheim’, they develop directly on last year’s long shoots. These spirea are pruned after flowering in the first half of June. Then, the plant will have time in the same growing season to produce shoots on which it will set inflorescence buds for next year’s spring. In these taxa, pruning cannot be postponed to the autumn date, as it would result in the complete loss of next year’s flowers. However, matching the date of harvesting shoots with accumulated metals with the date of cutting shrubs consistent with horticultural practice is also not without a phytoremediation assumption. The results show that the concentration of heavy metals in leaves in autumn is not always higher than in spring. For example, the average content of lead in the leaves of S. nipponica ‘Snowmound’ was 4.17 mg kg−1 d.m. in spring (with the content in soil at 1.95 mg kg−1 d.m.; BCF 2.14), and in autumn the content in leaves was 3.63 mg kg−1 d.m. (in soil 2.52 mg kg−1 d.m.; BCF 1.44). The average cadmium content in the leaves of S. × cinerea ‘Grefsheim’ in spring was 1.52 mg kg−1 d.m. (0.20 mg kg−1 d.m. in soil; BCF 7.82), and in autumn was 1.04 mg kg−1 d.m. and 0.22 mg kg−1 d.m., respectively (BCF 4.76). Both examples indicate that for some heavy metals and taxa of spirea, spring harvesting of leafy shoots may be more advantageous than autumn harvesting. Nonetheless, the developmental peculiarities of individual spirea species make it possible to use both dates in a targeted soil treatment measure.
The use of ornamental shrubs for remediation purposes in green spaces can effectively combine the aesthetic needs of residents with those of caring for the urban environment. At the same time, these shrubs do not necessarily have to have the status of hyperaccumulators, as it is possible in their case to implement a strategy based on less accumulation of metals but high biomass production [28]. It is worth noting that the genus Spiraea has many representatives in Polish and foreign dendrological collections, and it is not excluded that some species may prove to be extremely effective in soil phytoremediation processes. The dual function that the plants could perform would undoubtedly be an added value for urban green areas.
Based on the results of the soil analysis, it can be concluded that the degree of salinity of the selected sites for the cultivation of spirea in Poznań, Gdańsk and Lublin does not translate into excessive stress for the shrubs growing there. No damage to the cultivated spirea caused by growth in a saline environment was recorded at any of the studied sites. Komosa [46] includes blue-green and then browning and drying of leaves, soaring habit, limited growth of aboveground organs, or brittleness and ease of falling of blades. The chlorosis of leaves and dying shoots mentioned by Łuczak et al. [43] mentions salt damage to plants. Of the 48 mixed samples taken from locations in Poznań, the highest salinity was 0.401 mS cm−1, and the lowest was 0.163 mS cm−1, while the average value was 0.246 mS cm−1. For Lublin, on the other hand, the highest value of EC was 0.530 mS cm−1, the lowest was 0.190 mS cm−1, and the average was 0.257 mS cm−1. Meanwhile, for Gdansk, it was 0.471 mS cm−1, 0.124 mS cm−1, and 0.236 mS cm−1, respectively (Table 2 and Table 3). These results are several times lower than the literature values [47,48] at which damage occurred in spirea. In Marosz [47] experiment, S. × cinerea ‘Grefsheim’ responded strongly with a reduction in growth and development only at an EC of 6 mS cm−1, and at 12 mS cm−1 1/3 of the analyzed specimens died—the taxon was classified as a plant with strong resistance to substrate salinity, which is suitable for street plantings.
Sun et al. [48] presented the results of an 8-week experiment during which S. betulifolia, S. japonica, S. media, S. nipponica, and S. thunbergii were watered with a solution of NaCl and CaCl2 in two combinations—an EC of 3 mS cm−1 and an EC of 6 mS cm−1. Except for S. thunbergii, which had slightly damaged leaves, all specimens of the other species survived the two-month application period of the 3 mS cm−1 solution and maintained good health. In the case of shrubs treated with the 6 mS cm−1 solution, all specimens of S. thunbergii died and S. media suffered severe leaf damage, and S. betulifolia, S. japonica and S. nipponica showed slight to moderate blade damage and a significant reduction in shoot dry weight.
The results of our study from the three cities are similar, both in terms of salinity and soil reaction, with a marked alkalinization of the substrate. Of the eight sites for the cultivation of spirea in Lublin, eight in Gdansk, and 12 in Poznań, as many as 22 had an alkaline soil reaction, and the rest were neutral. Such soil properties were also noted in studies conducted in Kielce, Cracow and Warsaw [54,55,56]. This is undoubtedly a characteristic feature of the land of urban agglomerations, which (as explained by Czarnowska [57] and Breś [58]) is due to the precipitation of alkaline dust from low emissions, salinity and admixture of calcium debris.
The lack of specific recommendations in the literature regarding the cultivation requirements of spirea in terms of soil pH limits the interpretation of the results. To date, the result of only one experiment documenting the growth of two American species (S. alba and S. tomentosa) in soils with different pH has been published [59]. The authors checked growth, leaf nutrient content and degree of greening for three combinations of pH (in H2O)—6, 6.5 and 7—while reporting that the soil at their natural sites had a pH in the range of 4 to 6. The cited study showed that at the highest pH analyzed, the plants were lower and narrower than the shrubs from the other variants, although their leaf mass and degree of greening were the same as in the other combinations. As pH increased, the content of some nutrients in the blades (N, K, Zn, Mn) also decreased. Both spirea were evaluated as species that perform well outside their optimum, i.e., the soil in the area of their natural range. It is noteworthy that the lowest recorded soil pH at spirea growing sites in Poznań was 6.96, the highest was 8.51, and the average value was 7.69. In contrast, for Lublin, it was 7.36, 8.09 and 7.76, and for Gdańsk, it was 7.28, 8.40 and 7.96, respectively. The pH (in H2O) in the range of 6 to 6.5 is considered the optimum for most crops, including useful and ornamental plants [46]. It would follow that urban soils are not the best environment for plant growth, and creating more favorable conditions would require deliberate acidification. The situation could be improved by applying sulfur fertilizers annually, which would lower the soil reaction in the long run [60]. A possible solution is also the selection of species that naturally occur on land with neutral and alkaline pH. Analyzing the pH of China’s soils, it can be seen that the provinces of Shandong, Henan, Shanxi, Shaanxi, Gansu, Inner Mongolia Autonomous Region, Qinghai, Xinjiang and Tibet, together accounting for about half of the country’s area, have soils with pH (in H2O) ranging from 7.2 to 8.5 [61]. In such a vast area, there are natural stands of many spirea [62].

5. Conclusions

1. The taxa studied meet the basic requirements for plants used for soil phytoremediation processes, especially for chromium phytoextraction. Further laboratory studies are advisable (environment intentionally contaminated with heavy metals, varying increasing concentrations of individual metals), as well as on heavily contaminated sites, to confirm the usefulness of Spiraea taxa in heavy metal phytoextraction.
2. The degree of soil salinity of the studied sites of cultivation of spirea does not pose a threat to the shrubs growing there.
3. Most of the sites for the cultivation of spirea are characterized by an alkaline soil reaction, which, although not optimal for the growth of many plant species, is suitable for the cultivation of a number of spirea especially.
4. For the determination of the higher contents of Fe, Mn, Ni, Zn, Cd, Cr and Pb, the spring sampling date of spirea leaves is more appropriate.

Author Contributions

Conceptualization, W.A., M.B. and M.S.; methodology, M.B. and M.S.; material preparation, data collection and analysis, M.S. and M.B.; chemical analysis, M.B.; data curation, M.S.; writing—original draft preparation, M.S., W.A. and M.B.; writing—review and editing, W.A. and M.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in this study are included in the article; further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agriculture 14 01916 g001
Figure 1. Bioconcentration coefficient of selected heavy metals in the leaves of spirea—(a) spring, (b) autumn, (c) mean.
Figure 1. Bioconcentration coefficient of selected heavy metals in the leaves of spirea—(a) spring, (b) autumn, (c) mean.
Agriculture 14 01916 g001
Table 1. Heavy metal content in the soil of the cultivation sites of S. × cinerea ‘Grefsheim’, S. nipponica ‘Snowmound’, S. splendens and S. × vanhouttei in their leaves.
Table 1. Heavy metal content in the soil of the cultivation sites of S. × cinerea ‘Grefsheim’, S. nipponica ‘Snowmound’, S. splendens and S. × vanhouttei in their leaves.
CuFeMnNiZnCdCrPb
S. × cinerea ‘Grefsheim’soils (mg kg−1 d.m.)
Min.1.8239.263.460.094.780.070.151.25
Max.6.2179.109.320.2818.230.801.969.45
Mean3.6365.576.480.1511.890.210.914.53
SD *1.6814.042.170.064.120.200.623.24
CV **46.2821.4133.4940.0034.6595.2468.1371.52
leaves (mg kg−1 d.m.)
Min.4.67284.0731.001.1833.700.837.022.60
Max.14.42541.1398.642.1392.041.9819.614.73
Mean8.90405.5156.291.6455.931.2812.413.88
SD3.5490.5521.950.3319.520.374.380.83
CV39.7822.3338.9920.1234.9028.9135.2921.39
S. nipponica ‘Snowmound’soils (mg kg−1 d.m.)
Min.0.5643.403.830.003.560.160.001.03
Max.4.4370.117.850.2113.650.322.673.90
Mean2.3953.896.660.129.240.231.262.23
SD1.508.571.320.083.110.051.170.94
CV62.7615.9019.8266.6733.6621.7492.8642.15
leaves (mg kg−1 d.m.)
Min.3.95194.3631.430.6416.460.946.433.00
Max.7.04378.4648.611.1519.561.7518.814.90
Mean5.10279.5539.840.9417.931.3512.953.90
SD1.1060.425.590.180.960.324.540.60
CV21.5721.6114.0319.155.3523.7035.0615.38
S. splendenssoils (mg kg−1 d.m.)
Min.0.6325.452.970.037.100.110.181.11
Max.5.5388.5111.110.2416.020.301.644.57
Mean2.6657.335.760.1410.300.180.752.27
SD1.5223.682.830.073.160.070.491.19
CV57.1441.3049.1350.0030.6838.8965.3352.42
leaves (mg kg−1 d.m.)
Min.3.04218.2735.900.7419.630.835.802.71
Max.11.45507.75109.321.9230.111.8216.704.86
Mean7.04354.3261.391.3225.671.3510.763.97
SD3.1198.3923.540.413.430.374.060.74
CV44.1827.7738.3531.0613.3627.4137.7318.64
S. × vanhoutteisoils (mg kg−1 d.m.)
Min.2.5438.702.780.078.130.100.280.67
Max.6.0890.1012.430.3323.450.340.9712.85
Mean4.2859.677.500.1915.090.220.636.94
SD1.0218.424.250.095.050.080.264.34
CV23.8330.8756.6747.3733.4736.3641.2762.54
leaves (mg kg−1 d.m.)
Min.3.34195.9947.480.9431.290.754.292.69
Max.7.93398.18111.001.5850.101.6112.793.83
Mean5.53279.8878.501.2839.111.157.853.16
SD1.6363.7321.470.216.390.282.880.36
CV29.4822.7727.3516.4116.3424.3536.6911.39
* SD—standard deviation; ** CV—coefficient of variation.
Table 2. Average content of heavy metals (mg kg−1 d.m.) in the soils of the cultivation sites of S. × cinerea ‘Grefsheim’, S. nipponica ‘Snowmound’, S. splendens and S. × vanhouttei, depending on the date of soil sampling.
Table 2. Average content of heavy metals (mg kg−1 d.m.) in the soils of the cultivation sites of S. × cinerea ‘Grefsheim’, S. nipponica ‘Snowmound’, S. splendens and S. × vanhouttei, depending on the date of soil sampling.
MetalDate of Soil SamplingS. × cinerea ‘Grefsheim’S. nipponica ‘Snowmound’S. splendensS. × vanhoutteiŚrednia
Cuspring3.65 b*3.10 ab3.67 b4.67 b3.77 b
autumn3.60 b1.69 a1.65 a3.88 b2.71 a
mean3.63 bc2.39 a2.66 ab4.28 c
Fespring57.42 bc54.59 ab38.17 a53.29 ab50.87 a
autumn73.72 cd53.18 ab76.50 d66.06 bcd67.36 b
mean65.57 a53.89 a57.33 a59.67 a
Mnspring7.26 a6.13 a5.14 a6.16 a6.17 a
autumn5.71 a7.20 a6.38 a8.84 a7.03 a
mean6.48 a6.66 a5.76 a7.50 a
Nispring0.19 bc0.18 bc0.20 c0.18 bc0.19 b
autumn0.12 ab0.06 a0.08 a0.21 c0.12 a
mean0.15 ab0.12 a0.14 ab0.19 b
Znspring11.77 abc9.43 ab11.07 abc15.65 c11.98 a
autumn12.02 abc9.05 a9.53 ab14.53 bc11.28 a
mean11.89 ab9.24 a10.30 a15.09 b
Cdspring0.20 a0.24 a0.23 a0.24 a0.23 a
autumn0.22 a0.21 a0.14 a0.21 a0.19 a
mean0.21 a0.23 a0.18 a0.22 a
Crspring1.42 c2.37 d1.13 bc0.85 b1.44 b
autumn0.40 a0.16 a0.37 a0.42 a0.34 a
mean0.91 b1.26 c0.75 ab0.63 a
Pbspring4.20 ab1.95 a2.18 a6.50 b3.71 a
autumn4.86 ab2.52 a2.36 a7.38 b4.28 a
mean4.53 ab2.23 a2.27 a6.94 b
* Followed by the same letters do not differ significantly at α = 0.05 .
Table 3. Average heavy metal content (mg kg−1 d.m.) in leaves of S. × cinerea ‘Grefsheim’, S. nipponica, ‘Snowmound’, S. splendens and S. × vanhouttei depending on the date of leaf sampling.
Table 3. Average heavy metal content (mg kg−1 d.m.) in leaves of S. × cinerea ‘Grefsheim’, S. nipponica, ‘Snowmound’, S. splendens and S. × vanhouttei depending on the date of leaf sampling.
MetalDate of Leaf SamplingS. × cinerea ‘Grefsheim’S. nipponica ‘Snowmound’S. splendensS. × vanhoutteiŚrednia
Cuspring9.40 c*5.49 ab7.57 abc5.79 ab7.06 a
autumn8.40 bc4.72 a6.52 abc5.27 ab6.23 a
mean8.90 b5.10 a7.04 ab5.53 a
Fespring474.74 c326.96 b424.34 c323.56 b387.40 b
autumn336.28 b232.15 a284.30 ab236.20 a272.23 a
mean405.51 c279.55 a354.32 b279.88 a
Mnspring69.77 c44.52 ab76.74 c95.15 d71.54 b
autumn42.81 a35.17 a46.04 ab61.85 bc46.47 a
mean56.29 b39.84 a61.39 b78.50 c
Nispring1.78 d1.00 ab1.44 cd1.35 bc1.39 b
autumn1.50 cd0.88 a1.20 abc1.21 abc1.20 a
mean1.64 c0.94 a1.32 b1.28 b
Znspring61.52 e18.64 a26.74 ab43.94 cd37.71 b
autumn50.34 de17.21 a24.60 ab34.36 bc31.63 a
mean55.93 c17.93 a25.67 a39.15 b
Cdspring1.53 bc1.64 c1.63 c1.37 b1.54 b
autumn1.04 a1.07 a1.06 a0.93 a1.02 a
mean1.28 ab1.35 b1.35 b1.15 a
Crspring16.22 c15.79 c13.84 c10.26 b14.03 b
autumn8.60 b10.11 b7.68 ab5.44 a7.96 a
mean12.41 b12.95 b10.76 b7.85 a
Pbspring4.09 bc4.17 c4.22 c3.32 ab3.95 b
autumn3.68 abc3.63 abc3.72 abc2.99 a3.50 a
mean3.88 b3.90 b3.97 b3.16 a
* Followed by the same letters do not differ significantly at α = 0.05 .
Table 4. Soil reaction and salinity of spirea growing sites in Poznań.
Table 4. Soil reaction and salinity of spirea growing sites in Poznań.
Taxon/Street, LocationSample No.Spring TermAutumn Term
pH (H2O)EC (mS cm−1)pH (H2O)EC (mS cm−1)
S. × cinerea ‘Grefsheim’Karola Libelta
52.4124, 16.9189		2A-17.380.2337.930.260
2A-27.400.2457.890.256
Polska
52.4197, 16.8727		2B-17.320.1677.850.169
2B-27.350.1787.850.163
Żeromskiego
52.4165, 16.8923		2C-17.880.3787.770.249
2C-27.770.4017.800.241
S. splendensRondo Śródka
52.4102, 16.9561		3A-17.590.2877.670.255
3A-27.610.2937.630.254
Garbary
52.4101, 16.9381		3B-17.810.3527.740.230
3B-27.890.3477.710.228
Strzeszyńska
52.4513, 16.8891		3C-18.110.2697.500.250
3C-28.060.2977.490.251
S. nipponica ‘Snowmound’Winogrady
52.4249, 16.9271		4A-17.840.2097.720.260
4A-27.910.1977.700.263
Lechicka
52.4381, 16.9529		4B-17.760.2637.950.235
4B-27.890.2677.890.230
Polska
52.4184, 16.8717		4C-17.790.2827.700.222
4C-27.840.2917.720.227
S. × vanhoutteiSłowiańska
52.4302, 16.9287		1A-17.360.1856.960.171
1A-27.280.2106.980.168
Serbska
52.4332, 16.9430		1B-17.550.2847.370.180
1B-27.510.2787.300.182
Lechicka
52.4396, 16.9506		1C-17.660.2468.510.227
1C-27.560.2568.480.229
Table 5. Soil reaction and salinity of spirea growing sites in Lublin and Gdańsk (summer term).
Table 5. Soil reaction and salinity of spirea growing sites in Lublin and Gdańsk (summer term).
TaxonStreet, LocationpH
(H2O)		EC
(mS cm−1)
Lublin
S. × cinerea ‘Grefsheim’Aleja Wincentego Witosa 51.2304, 22.61287.850.258
S. splendensNadbystrzycka 51.2358, 22.54677.900.220
S. × vanhoutteiWyżynna 51.2239, 22.52567.690.216
S. × vanhoutteiPogodna 51.2335, 22.59507.670.190
Gdańsk
S. × cinerea ‘Grefsheim’Aleja Grunwaldzka 54.3779, 18.60837.890.258
S. splendensAleja Rzeczypospolitej 54.4029, 18.59178.150.148
S. × vanhoutteiWały Jagiellońskie 54.3561, 18.64567.280.471
S. × vanhoutteiAleja Rzeczypospolitej 54.4032, 18.59178.190.178
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Antkowiak, W.; Bosiacki, M.; Sowelo, M. Potential of Selected Species of Spiraea L. for Phytoremediation of Heavy Metals from Soils of Urban Areas. Agriculture 2024, 14, 1916. https://doi.org/10.3390/agriculture14111916

AMA Style

Antkowiak W, Bosiacki M, Sowelo M. Potential of Selected Species of Spiraea L. for Phytoremediation of Heavy Metals from Soils of Urban Areas. Agriculture. 2024; 14(11):1916. https://doi.org/10.3390/agriculture14111916

Chicago/Turabian Style

Antkowiak, Wojciech, Maciej Bosiacki, and Mateusz Sowelo. 2024. "Potential of Selected Species of Spiraea L. for Phytoremediation of Heavy Metals from Soils of Urban Areas" Agriculture 14, no. 11: 1916. https://doi.org/10.3390/agriculture14111916

APA Style

Antkowiak, W., Bosiacki, M., & Sowelo, M. (2024). Potential of Selected Species of Spiraea L. for Phytoremediation of Heavy Metals from Soils of Urban Areas. Agriculture, 14(11), 1916. https://doi.org/10.3390/agriculture14111916

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