Environ Monit Assess (2017) 189:34 DOI 10.1007/s10661-016-5740-2

Pollution in the urban soils of , China, evaluated using a pollution index, mobility of heavy metals, and enzymatic activities

Yu LI & Hong-guan LI & Fu-cheng LIU

Received: 12 September 2016 /Accepted: 5 December 2016 # Springer International Publishing Switzerland 2016

Abstract Soil samples from 16 urban sites in Lianyun- Lianyungang soils was Cd > Zn > Pb > Cu > As > Cr. gang, China were collected and analyzed. A pollution Soil urease activity, alkaline phosphatase activity, and index was used to assess the potential ecological risk of invertase activity varied considerably in different pollu- heavy metals and a sequential extraction procedure was tion degree sites. Soil enzyme activities had the lowest used to evaluate the relative distribution of Cu, Zn, Pb, levels in roadside and industrial regions. Across all the Cd, Cr, and As in exchangeable, carbonate, Fe/Mn soil data in the five regions, the total Cu, Zn, Pb, Cd, Cr, oxide, organic/sulfide, and residual fractions. The mo- and As level was negatively correlated with urease bility of heavy metals and urease (URE) activity, alka- activity, alkaline phosphatase activity, and invertase ac- line phosphatase (ALP) activity, and invertase (INV) tivity, but the relationship was not significant. In the activity of soils was determined. The results showed industrial region, alkaline phosphatase activity had sig- that the average concentrations of Cu, Zn, Pb, Cd, Cr, nificant negative correlations with total Cu, Pb, Cr, Zn, and As in Lianyungang soils were much higher than Cd, and heavy metal fractions. This showed that alkaline those in the coastal city soil background values of Jiang- phosphatase activity was sensitive to heavy metals in su and China. Among the five studied regions (utilities, heavily contaminated regions, whereas urease and in- commercial, industrial, tourism, and roadside), the in- vertase were less affected. The combination of the var- dustrial region had the highest metal concentrations ious methods may offer a powerful analytical technique demonstrating that land use had a significant impact in the study of heavy metal pollution in street soil. on the accumulation of heavy metals in Lianyungang soils. Compared to the other metals, Cd showed the Keywords Heavy metals . Urban soils . Partitioning and highest ecological risk. According to chemical mobility. Enzymatic activities . Lianyungang partitioning, Cu was associated with the organic/ sulfides and Pb and Zn were mainly in the carbonate and the Fe/Mn oxide phase. The greatest amounts of Cd Introduction were found in exchangeable and carbonate fractions, while Cr and As were mainly in the residual fraction. Environmental quality is of vital importance to the Cd had the highest mobility of all metals, and the order health of humans living in cities (Figueiredo et al. of mobility (highest to lowest) of heavy metals in 2009). Vehicle emissions, industrial discharges, domes- tic heating, and other anthropogenic activities pollute air, water, and soil in urban areas (Mahanta and Y. LI (*) : H.

Christoforidis and Stamatis 2009). Heavy metal pollut- using sequential extraction procedures; and (3) examine ants (Cd, Cu, Pb, Zn, Hg, and As) are especially danger- the relationship between enzymatic activity and heavy ous due to their toxicity and environmental persistence metal concentration in soils within different areas of (Sheng et al. 2012). The presence of heavy metals in Lianyungang. urban soils is a serious environmental concern due to their persistence and long half-lives within the human body (Wei and Yang 2010; Mahanta and Bhattacharyya Materials and methods 2011; Crnković et al., 2006). Pollutants introduced into the soil also change the enzymatic activities of microbiota Study location (Baran et al. 2004). Soil enzyme activities reflect the dynamics of microbial metabolic processes associated Lianyungang is located on the coast of the Yellow Sea in with nutrient cycling and are sensitive indicators of envi- northern Province with geographic coordinates of ronmental stresses caused by soil quality degradation 34°~35°07′ N, 118°24′~119°48′ E. The urban area of (Wang et al. 2011). Hao et al. (2009) showed that the Lianyungang has three districts: Xinpu, Haizhou, and total soil N had a significant positive linear relationship Xugou. Most of the central commercial and traditional with urease activity, and organic matter contents affected residential areas are located in the Xinpu —the main invertase activity in urban soils at Shanghai City. Dar city zone. The industrial activities are concentrated in the (1996) and Moreno et al. (2001) reported that the Cd Haizhou district—an old city zone. Due to the develop- toxicity decreased alkaline phosphatase and urease activ- ment of a marine-based economy, rapid urbanization has ity in different soils. Heavy metal inhibition of enzymatic occurredintheXugoudistrict—a harbor zone, which reactions occurs by binding to the substrate, combining consists of residential, industrial, and commercial sites. with the protein-active groups of the enzymes, or reacting with enzyme-substrate complexes (Papa et al. 2010). Many studies have documented heavy metal pollution Sample collection and chemical analysis in urban soils of locations such as Korea, Nigeria, Bir- mingham (UK), Hermosillo (Mexico), Amman (Jordan), A total of 16 roadside soils from three urban districts of Guwahati (India), and many (>20) cities in China Lianyungang were collected in May 2014. Description of (Charlesworth et al. 2003; Han et al. 2006; Meza- the sampling sites is shown in Table 1. There were five Figueroa et al., 2007; Duong and Lee 2009; Wei and Yang type abbreviations of sampling locations, including public 2010; Mahanta and Bhattacharyya 2011;Akanetal. utilities (park, school, train station, and hospital), commer- 2013). The different city characteristics related to econom- cial, industrial, tourism-related, and roadsides. These are ic progress, population size, industrial activities, traffic showninFig.1. About 10 g of the top 10-cm layer of soil conditions, etc., have resulted in significant differences in was collected approximately 3 m from the paved edge of pollution. Total analysis of heavy metals in soils is a useful the road using a stainless steel shovel. A total of 4–5soil parameter concerning possible contamination, but the samples were taken and then mixed thoroughly to obtain chemical form of the metals determines their mobility one bulk sample for each sampling site (Shi et al. 2008). and bioavailability. Heavy metal chemistry provides The soil samples were maintained in self-sealing plastic criteria for estimating their potential environmental and bags. One half of the soil samples were air-dried prior to biological effects in urban soils (Harrison et al. 1981;Lu determination of enzymatic activities. The other samples et al. 2007). were oven-dried at 40°C for 48 h, and then stones and There has been little research on the urban soils of interfering materials were removed by passing the soil Lianyungang City, China. Lianyungang is a coastal city through a 63-μm mesh nylon sieve. This smaller particle in the northern Jiangsu Province, and no data are available fraction has often been studied because it is a good metal about heavy metals and enzyme characteristics in soils adsorption carrier and it represents a relatively greater there. Our study objectives were to (1) determine the total human health hazard (Duggan and Inskip 1985; Whicker content and distribution of Cu, Zn, Pb, Cd, Cr, and As in et al. 1997; Christoforidis and Stamatis 2009). To reduce soils from different areas of Lianyungang and assess the potential contamination, all procedures—including the heavy metal contamination in soils related to the pollution treatment of sample collection and analyses—were care- index; (2) evaluate the mobility of heavy metals in soils fully undertaken. Environ Monit Assess (2017) 189:34 Page 3 of 13 34

Table 1 Name and type of location of sample collection site of Lianyungang city, China

Sample no. DMS (N–E) Sample code Location Location type

134°35′59.8″–119 °11′24.5″ S1 Cangwu park Utilities 234°35′51.9″–119 °10″38.6″ S2 Jiefangroad primary school Utilities 334°36′04.8″–119 °10′27.3″ S3 Buxing street Commercial 434°36′31.1″–119 °09′34.7″ S4 Train station Utilities 534°34′56.7″–119 °09′24.8″ S5 Qingnian park Utilities 634°34′57.7″–119 °08′42.0″ S6 Debang chemical plant Industrial 734°34″49.6′–119 °07′50.3″ S7 Xinhai power plant Industrial 834°34′18.1″–119 °08′02.7″ S8 Haizhou Drum-tower Commercial 934°33′59.2″–119 °10′23.3″ S9 Kongwang mountain Touristic 10 34°44′05.2″–119 °20′00.0′ S10 Soda plant Industrial 11 34°45′49.8″–119 °22′32.3″ S11 West Breakwater Roadside 12 34°45′00.3″–119 °21′57.2″ S12 149 Hospital Utilities 13 34°44′32.2″–119 °24′27.9″ S13 Lianyungang harbor Industrial 14 34°39′14.5″–119 °14′36.7″ S14 Huaguoshan village Roadside 15 34°38′35.3″–119 °14′28.5″ S15 Huaguoshan mountain Touristic 16 34°36′16.9″–119 °13′38.9″ S16 Huaguoshan road Roadside

DMS (N–E)degreeminutesecond(North–East) of geographic coordinates of the sampling sites, S soil

Samples for heavy metal analyses were completely Teflon systems, and then concentrations of the metals digested with a mixture of HF-HNO3-HClO4 in closed Cu, Zn, Pb, Cd, Cr, and As were determined using an

Fig. 1 Map of sample sites in Lianyungang city, with a vicinity map showing the location within China 34 Page 4 of 13 Environ Monit Assess (2017) 189:34

Inductively Coupled Plasma Atomic Emission Spec- Results trometer (ICP-AES). The accuracy and precision of the analytical procedures were checked through analysis of Total metal concentrations in urban soils reference sediment material GBW07408 (GSS-8). The accuracy and bias of metals for the reference sample The concentration of metals (mean, range) in urban soil were about 5%, respectively, and were considered satis- samples from five types of locations in Lianyungang are factory for the environmental analyses of this study. showninTable2. Coastal city soil background values of Chemical separation of heavy metals in urban samples Jiangsu (Xia et al., 1987) and China (CNEMC 1990)were was achieved using a five-step sequential extraction used as reference values. The mean levels of the six procedure (Tessier et al. 1979). Heavy metals in road- measured metals in urban soils exceeded the reference side samples were successively extracted as exchange- values, clearly demonstrating an anthropogenic contribu- able (F1), bound to carbonate phase (F2), bound to tion. The highest concentrations of Cu, Zn, Pb, Cd, and Cr reducible phases (iron and manganese oxides) (F3), in urban soils were observed at Lianyungang Harbor, bound to organic matter and sulfides (F4), and residual while the highest levels of As were found in soil from or lattice metals (F5). All of the measurements were West Breakwater. The main activities at Lianyungang carried out in triplicate. Harbor involve shipments of containers, petroleum coke, Enzymatic activities were determined according to coal, and ores, which caused urban soils heavily polluted methods used by Guan (1986). Urease activity, with oil, metal mine dusts, and waste gases around Lian- expressed as mg N g−1 dry soil 24 h−1, was measured yungang Harbor (Huang 2002). It is possible that indus- by the indophenol colorimetric method. Invertase activ- trial emissions of metals may cause substantial pollution ity was measured by the 3, 5-dinitrosalicylic acid meth- of dusts at Lianyungang Harbor. West Breakwater is a od and expressed as mg glucose g−1 dry soil 24 h−1. Soil dike between Xugou land and Lian island, which was alkaline phosphatase activity was measured spectropho- founded by reclaiming land from marine cultivating area tometrically by the disodium phenyl phosphate method (Xu 2005). So arsenical pesticides and fertilizers used in and expressed as mg phenol produced g−1 dry soil mariculture and road greening activities may cause As 12 h−1. enrichment. Cu contents in soils in the five types of Pearson correlation coefficients were performed land use varied between 26.68 to 283.1 mg/kg, and using SPSS 20.0. mean Cu values were in the order of (high to low)

Table 2 Summary of total concentrations of Cu, Zn, Pb, Cd, Cr, and As in urban soils in Lianyungang (mg/kg)

Region Parameter Cu Zn Pb Cd Cr As

Utilities Range 46.05–111.7 453.4–749.0 25.45–265.3 0.43–1.52 50.5–163.5 1.68–18.46 Mean 62.98 544.9 81.53 0.76 96.28 7.96 Commercial Range 68.18–89.69 547.7–580.2 38.54–55.07 0.55–0.56 77.94–99.97 7.84–13.81 Mean 78.94 564.0 46.80 0.56 88.96 10.82 Industrial Range 26.68–283.1 10.61–1851 9.51–498.5 nd—3.71 0.91–3260 nd—11.26 Mean 110.5 699.0 155.4 1.23 872.6 2.82 Touristic Range 51.53–51.76 476.1–714.7 34.89–37.15 0.38–0.54 66.31–85.95 nd—6.00 Mean 51.64 595.4 36.02 0.46 76.13 3.00 Roadside Range 36.66–84.36 455.6–577.7 40.12–389.6 0.31–1.70 111.0–114.6 0.46–66.58 Mean 57.77 574.9 161.4 0.84 112.8 31.01 Background values of Chinaa 22.6 74.2 26 0.097 61 11.2 Background values of Jiangsub 15.84 64.68 24.7 0.065 60.28 8.59 nd not detectable a CNEMC (1990) b Xia et al. (1987) Environ Monit Assess (2017) 189:34 Page 5 of 13 34

Table 3 The mean levels of heavy metal concentrations (mg/kg) in urban soils from other countries or cities

Area Cu Zn Pb Cd Cr As Reference

Lianyungang 74.46 597.8 104.9 0.88 290.0 14.31 This study Hongkong 23.3 125 94.6 0.62 23.1 Li et al. (2004) Belgrade 28.3 118 55.5 32.1 7.2 Crnković et al. (2006) Beijing 23.7 65.6 28.6 0.15 35.6 Zheng et al. (2008) Shanghai 59.25 301.4 70.69 0.52 107.9 Shi et al.(2008) Qingdao 55.0 201 62 54 Yao et al. (2008) Annaba 39 67.5 53.1 0.44 30.9 Maas et al., 2010 Guwahati 124.4 286 170.5 18.0 122.9 Mahanta and Bhattacharyya (2011) Novi Sad 21.9 111 28.8 1.59 3.33 Škrbić and Đurišić-Mladenović (2013) industrial > commercial > utilities > roadside > tourism. showed that ore dusts, industrial operations, and traf- Compared to other locations (Table 3), the mean Cu fic emissions contributed to the highest Pb enrich- level in Lianyungang urban soils was much higher ment in Lianyungang street soils. The highest level of than levels in Beijing (China), Shanghai (China), Cd was found in Lianyungang Harbor soil (3.71 mg/ Belgrade (Serbia and Montenegro), Hongkong (Chi- kg), followed by soil from West Breakwater na), Qingdao (China), Novi Sad (Serbia), and Anna- (1.70 mg/kg), and 149 Hospital (1.52 mg/kg). The ba (Algeria), but lower than that in Guwahati (India). mean values in different locations were much lower Zn also had the highest mean levels in industrial than results in Guwahati and Novi Sad (Mahanta and areas, and Zn in soils from utilities, commercial, Bhattacharyya 2011; Crnković et al., 2006). Distri- roadside, and tourism sites had similar mean content. bution of Cr levels in the study area soils ranged from The mean concentration of Zn in this study was 0.91 to 3260 mg/kg, with a mean of 290.0 mg/kg. higher than that reported in other studies (Table 3). This was much higher than values found in other Pb had the highest mean level in the roadside site and countries or cities. As had the highest concentrations was highly variable among the five locations. The in soils from roadside sites followed by commercial mean values of Pb were (high to low) roadside > in- areas. As levels in urban soil of Lianyungang were dustrial > utilities > commercial > tourism, which higher than those in Belgrade (Crnković et al., 2006).

Table 4 Concentrations of heavy metal fractions in soil samples in Lianyungang (mg/kg)

Heavy metals Exchangeable Carbonate Fe/Mn oxide Organic/sulfide Residue

Cu Range 2.12–6.56 2.93–39.63 6.14–70.78 11.47–124.6 4.00–45.30 Mean ± S.D 3.88 ± 1.32 8.43 ± 8.75 16.71 ± 15.09 32.21 ± 26.52 13.74 ± 10.00 Zn Range 1.07–55.89 1.87–292.4 4.13–762.6 0.59–125.5 3.40–614.5 Mean ± S. D 20.37 ± 13.05 99.41 ± 58.70 245.2 ± 152.4 36.90 ± 26.70 196.9 ± 126.6 Pb Range 1.25–25.33 1.26–60.82 3.92–209.4 1.59–94.22 2.18–123.6 Mean ± S. D 5.07 ± 6.32 12.72 ± 16.96 42.50 ± 59.61 18.31 ± 26.28 26.73 ± 37.82 Cd Range nd—2.27 nd—0.78 nd—0.5 nd—0.078 nd—0.18 Mean ± S. D 0.47 ± 0.54 0.18 ± 0.18 0.13 ± 0.12 0.024 ± 0.020 0.034 ± 0.046 Cr Range 0.032–111.8 0.038–115.4 0.081–430.3 0.056–67.78 0.71–2539 Mean ± S. D 10.28 ± 27.14 11.03 ± 27.91 41.86 ± 106.4 7.64 ± 16.18 226.3 ± 617.6 As Range nd—4.18 nd—3.92 nd—14.18 nd—1.99 nd—42.81 Mean ± S. D 0.64 ± 1.04 0.61 ± 0.99 2.23 ± 3.56 0.47 ± 0.57 6.79 ± 10.72 nd not detectable 34 Page 6 of 13 Environ Monit Assess (2017) 189:34

Zn 100% 100%

80% F5 80% F5 F4 F4 60% 60% F3 F3 40% F2 40% F2 20% F1 20% F1 Chemical forms (%) forms Chemical C h em ical fo rm s (% )

0% 0% 1 2 3 4 5 6 7 8 9 10111213141516 12345678910111213141516 Sampling points Sampling points

Pb Cd 100% 100%

80% F5 80% F5 F4 F4 60% 60% F3 F3 40% F2 40% F2 20% F1 20% F1 Chemical forms (%) forms Chemical Chemical forms (%) forms Chemical 0% 0% 12345678910111213141516 1 2 3 4 5 6 7 8 9 10111213141516 Sampling points Sampling points

Cr As 100% 100%

80% F5 80% F5 F4 F4 60% 60% F3 F3 40% F2 40% F2 20% F1 20% F1 C h em ical fo rm s(% ) C hem ical form s (% ) 0% 0% 1 2 3 4 5 6 7 8 9 10111213141516 12345678910111213141516 Sampling points Sampling points Fig. 2 Chemical forms of Cu, Zn, Pb, Cd, Cr, and As in Lianyungang urban soils

Heavy metal fractions in urban soils metals in the residual fraction (F5) are entrapped within the crystal structure of the minerals and represent the least The concentration ranges and the standard deviations of mobile fraction (Mahanta and Bhattacharyya 2011). The the fractions of Cu, Zn, Pb, Cd, Cr, and As in urban soils of distribution of Cu fractions in soil samples indicated that Lianyungang are shown in Table 4. The distribution of the highest proportion was associated with organic matter metals in the five fractions varied greatly among the sam- and sulfides (F4), averaging 42.97%. The lowest content ples (Fig. 2). Generally, heavy metals in the exchangeable (5.15%) was in exchangeable fraction (F1), and mean Cu and carbonate fractions (F1 + F2) are considered mobile, levels of 11.23, 22.29, and 18.32% were associated with while the reducible (F3) and oxidizable (F4) fractions are the carbonate phase (F2), Fe/Mn oxide phase (F3), and the relatively stable under normal soil conditions. Heavy residual fraction (F5). Zn had the highest percentages in the Environ Monit Assess (2017) 189:34 Page 7 of 13 34

Fe/Mn oxide phase (41.01%) and the residual fraction Enzymatic activity of urban soils (32.78%), while the carbonate phase (16.63%) was of minor importance. Pb had the following fraction order in Substantial spatial variation in enzyme activities was soil samples: Fe/Mn oxide (39.60%) > residual found in Lianyungang soils from the five regions (24.90%) > organic/sulfide (17.06%) > carbonate (Fig. 3). Soil urease activities ranged from 0.36 to (11.85%) > exchangeable (6.59%). Cd had over 93% in 4.09 mg NH4-N g−1 24 h−1 and were similar to results the first three fractions with the smaller amounts associated from urban soils (Hao et al. 2009). The highest with the organic/sulfide and residue fractions. These data urease value was from station 8 (Haizhou Drum-tower, were similar to other reports (Li et al. 2001;Luetal.2007). in the commercial region), while the lowest value was Cr had the highest content in the residue fraction (>70%) found at station 1 (Cangwu Park, in the utilities region) of soil samples; Fe/Mn oxide (about 10%) was of second- (Fig. 3). The mean soil urease activities in five regions ary importance, and a small proportion of Cr was found in were (high to low) commercial > tourism > industri- exchangeable and carbonate phases. Similar to Cr, the al > utilities > roadside. The soil alkaline phosphatase residue fraction (over 60%) was the most important frac- activities in this study ranged from 0.12 to 1.68 mg tion for As in soils, followed by Fe/Mn oxide. phenol produced g−1 12 h−1 and significantly differed

Fig. 3 Enzymatic activities of 4.5 4 urban soils from different stations ) 1 in Lianyungang − 3.5 3 24 h 1 − 2.5

-N g 2 4 1.5 urease activity 1 (mg NH 0.5 0 12345678910111213141516 station

1.8 ty 1.6 )

−1 1.4 1.2 24 h

−1 1 0.8 0.6 0.4 (mg phenol g phenol (mg

alkaline phosphatase activi phosphatase alkaline 0.2 0 12345678910111213141516 station

25 ) 1

− 20 24 h

−1 15

10 invertase activity 5 (mg glucose g glucose (mg

0 1 2 3 4 5 6 7 8 9 10111213141516 station 34 Page 8 of 13 Environ Monit Assess (2017) 189:34 between regions. The highest ALP value was from Lianyungang, an ecological risk index of the metals station 5 (Qingnian Park, in the utilities region), while was calculated using the following formulas the lowest ALP value was from station 13 (Lianyungang (Hakanson 1980): Harbor, in the industrial region) (Fig. 3). The mean soil : i ALP activities in five regions were (high to low) com- Contamination index of each element C f mercial > utilities > touristic > roadside > industrial. The i i ¼ Cn =Bb ð1Þ soil invertase activities in Lianyungang urban streets ranged from 0.50 to 21.08 mg glucose g−1 dry soil where Cn is the concentration of element in environ- 24 h−1, and were significantly different between the five ment, Bb is the background value. regions. The highest INV value was from station 8 as : i URE, while the lowest was from station 13 as ALP. The Ecological risk index of each heavy metal E f mean soil INV activities from the five regions were i i ¼ C f  T r ð2Þ (high to low) tourism > commercial > utilities > roadside > industrial. i where Tr means the toxic response factor of the selected metal. The ecological risk index of each sample associ- ated with heavy metal concentrations: Discussion

Assessment of potential ecological risk i RI ¼ ∑E f ð3Þ

The contamination from Cu, Zn, Cd, and Cr in urban soil usually originated from motor vehicle gasoline, car com- According to Hakanson (1980), the toxic response ponents, oil lubricants, and industrial and incinerator emis- factorsforCu,Zn,Pb,Cd,Cr,andAsare5,1,5,30,2, sions (Adriano 2001;Lietal.2001). Cd-containing phos- and 10, respectively. RI is calculated from the summation phate fertilizers also contributed to most of the Cd enrich- of all the values derived from the calculation of ecological i ment in city streets (Yesilonis et al. 2008). Prolonged risk for every metal (∑Ef ). Five categories of metal/ application of fertilizer containing Cd probably contributed sample pollution included low ecological risk (Ef <40, to the accumulation of Cd in the dust and soils of Lian- RI < 55), moderate ecological risk (40 ≤ Ef <80, yungang urban parks and the green belt. Pb, used as an 55 ≤ RI < 110), considerable ecological risk (80 ≤ Ef <160, ≤ ≤ antiknock agent in gasoline and in paints and car batteries, 110 RI < 220), high ecological risk (160 Ef <320, is a major source of pollution in cities (Lincoln et al. 2007). 220 ≤ RI < 440), and extreme high ecological risk

At least some As pollution has an agricultural origin from (Ef > 320, RI > 440) (Hakanson 1980;Shietal.2006). arsenical pesticides used in the green belt. The Cu, Zn, Pb, Cd, Cr, and As potential ecological risk Ecological risk index (RI) represents the sensitivity indexes in urban soils from different land types in Lian- of various biological communities to toxic substances yungang are presented in Table 5. The calculated Ef values and illustrates the potential ecological risk caused by of six selected heavy metals indicated that Cu, Zn, Pb, Cr, heavy metals (Sun et al. 2010). To assess the contami- and As in soils from five regions were in the low ecological nation levels of the metals in urban soils in risk category. However, Cd showed high/extreme high

Table 5 The heavy metal potential ecological risk indexes in urban soils in Lianyungang

Region Ef RI Pollution degree

Cu Zn Pb Cd Cr As

Utilities 19.88 8.42 16.50 351.7 3.19 9.27 409.0 High Commercial 24.91 8.72 9.47 256.2 2.95 12.60 314.8 High Industrial 34.89 10.81 31.45 566.5 28.95 3.28 675.9 Extremely high Touristic 16.30 9.20 7.29 212.3 2.52 3.49 251.1 High Roadside 18.24 8.89 32.66 386.2 3.74 36.10 485.8 Extremely high Environ Monit Assess (2017) 189:34 Page 9 of 13 34 ecological risk in five regions. Based on the RI values from had significantly higher concentrations in soil than the i Table 5, which was calculated by summation of the Cf background level. This indicated that these metals did not values for six heavy metals at sites from different types of originate from parent materials but from anthropogenic land use, the urban soils from industrial and roadside sites sources, such as industrial discharges, motor vehicle con- had extreme high potential ecological risk, and other ob- taminations, and inorganic fertilizers. served sites had high potential ecological risk.

Relationship between enzymatic activities and heavy Mobility of the metals in urban soils metals

The bioavailability and eco-toxicity of metals mainly de- The URE activity, ALP activity, and INV activity varied pend on their speciation (Sun et al. 2010). Heavy metals in considerably in sites with different degrees of pollution. partition fractions are considered potentially mobile in the Soil enzyme activities in roadside and industrial sites, with order (high to low) of exchangeable > carbonate > Fe/Mn an extremely high amount of pollution based on the heavy oxide > organic/sulfide > residual (Tessier et al., 1979). metal pollution indexes (Table 5), were lower than enzyme Exchangeable and carbonate-bound fractions are ready to activities from other sites. Enzyme reactions are inhibited be absorbed in plants or in water system causing pollution. by metals which may complex with the substrate, combine So, these fractions should be identified as direct effect with the protein-active groups of the enzymes, or react fraction, while the oxidizable fraction can be identified as with the enzyme-substrate complex (Hinojosa et al. 2004). potential effect fraction and residual fraction is identified as The heavy metal inhibition of soil enzymes was related to stable fraction (Sun et al. 2010). The different mobilities of land use in Lianyungang, and this corresponds to the metals have different bioavailability and environmental results of Papa et al. (2010). implications. Higher MF means higher mobility and higher The relationships between the heavy metals and en- metals’ availability to the biological systems (Olajire et al. zyme activities in soils from five regions are discussed. 2003; Huang et al. 2007). The mobility factor (MF) was Across all the data in 16 sites, total Cu, Zn, Pb, Cd, Cr, and calculated to assess metal mobility on the basis of the ratio As were negatively correlated with URE activity, ALP of exchangeable, carbonate-bound fractions to the sum of activity, and INVactivity, although these correlations were all fractions (Li et al. 2001; Yusuf 2007). The mobility of not statistically significant. However, negative correlations the heavy metals in soils is shown in Fig. 4. Considering indicate that the heavy metals are interfering with enzy- the first two extraction steps of the Tessier method, the matic expression in urban soils (Papa et al. 2010). Papa order of mobility of heavy metals in urban soils in Lian- et al. (2010) found negative correlation between some yungang was (high to low) Cd > Zn > Pb > Cu > As > Cr. enzyme activities and heavy metal contents in an urban Compared to the other metals, Cd had the highest mobility park of Caserta (Italy). Gülser and Erdoğan (2008)also (74.52%) in soils followed by Zn (20.62%), Pb (19.02%), found alkaline phosphatase and urease enzyme activities Cu (17.12%), As (11.51%), and Cr (7.63%). Lu et al. showing negative correlations with total heavy metal con- (2007) found that anthropogenic-derived heavy metals tents in roadside soils of intensive traffic regions of Van- were more mobile and represented a greater potential Turkey. Accordingly, URE activity, ALP activity, and biohazard in the environment. In this study, six metals INV activity of urban soils, here investigated, were

Fig. 4 Mean mobility factors 90 (MF) of Cu, Zn, Pb, Cd, Cr, As in 80 Lianyungang urban soils 70 60 50 40 30 Metal MF (%) 20 10 0 Cu Zn Pb Cd Cr As Metal 34 Page 10 of 13 Environ Monit Assess (2017) 189:34 negatively influenced by Cu, Zn, Pb, Cd, Cr, and As. In enzyme activities using different inhibition reactions and roadside region and industrial region sites with an ex- demonstrated that enzyme activities typically decrease tremely high degree of pollution, correlations between with increasing heavy metal concentrations (Kandeler total heavy metals and enzyme activities were determined. et al. 2000; Karaca et al. 2002). The effect of heavy metals In roadside sites, total soil Cu, Zn, Pb, Cd, Cr, and As on enzyme activities may vary considerably among the were negatively correlated with URE activity, ALP activ- elements, enzymes, and soils (Gianfreda et al. 2005). In ity, and INV activity but not significant statistically. In the this study, ALP activity was sensitive to several heavy industrial region, ALP activity had significant negative metals in the industrial region, whereas urease and inver- correlations with total Cu, Pb, and Cr content at P <0.05 tase were less affected. and the total Zn, Cd of soils at P <0.01(Table6). Several The metal fraction concentrations can provide a pre- studies have examined the effects of metals in soils on cise index representing the influence of heavy metal on soil microorganisms and enzyme activities (Ghosh et al. Table 6 Pearson correlation coefficients between enzymatic ac- 2004; Fernandez et al. 2005). In the industrial region, tivities and heavy metal fractions in soils in industrial region ALP activity was significantly correlated with the levels Metal Soil fractions URE ALP INV of heavy metal fractions (Table 6). Simple linear corre- lations across the industrial sites’ data showed that ALP Cu Cu-total −0.678 −0.987* −0.673 activity had a significant negative correlation with ex- Cu-F1 0.016 0.112 −0.134 tractable Cu, Zn, Pb, Cd, and Cr, as a result of the Cu-F2 −0.752 −0.963* −0.592 absolute concentration of fraction metals almost Cu-F3 −0.725 −0.971* −0.613 always increased as the concentration of total metal Cu-F4 −0.649 −0.990* −0.689 increased. Liu et al. (2002)andCaietal.(2005)reported Cu-F5 −0.578 −0.999** −0.775 that enzyme activities were closely related to heavy Zn Zn-total −0.644 −0.992** −0.730 metal fraction in soils. Li et al. (2010)demonstratedthat Zn-F1 −0.571 −0.987* −0.799 soil enzyme activities varied with the transformation of Zn-F2 −0.618 −0.993** −0.756 heavy metals from one fraction to another. The evalua- Zn-F3 −0.644 −0.992** −0.731 tion of the bioavailability of metals to environment is Zn-F4 −0.663 −0.990* −0.711 essential to predict changes in metal behavior in re- Zn-F5 −0.659 −0.990** −0.715 sponse to environment conditions (Sun et al. 2010). In Pb Pb-total −0.731 −0.971* −0.615 general, anthropogenic heavy metals are more easily Pb-F1 −0.610 −0.987* −0.697 mobile and potentially more bioavailable under most Pb-F2 −0.725 −0.974* −0.624 soil conditions, and as concentration of anthropogenic Pb-F3 −0.735 −0.970* −0.610 metals increase, they have increasing mobility or have a Pb-F4 −0.742 −0.967* −0.604 greater potential biohazard (Lu et al. 2007). The pres- Pb-F5 −0.726 −0.972* −0.618 ence of total and fraction metal concentrations negative- ly affected ALP activity and illustrated the potential Cd Cd-total −0.651 −0.990** −0.690 utility to determine soil contamination level using a soil Cd-F1 −0.793 −0.997 −0.654 indicator with biological function. Cd-F2 −0.938 −1.000** −0.716 Cd-F3 −0.792 −0.997 −0.656 Cd-F4 −0.695 −0.998* −0.758 Conclusions Cd-F5 −0.818 −0.992 −0.623 Cr Cr-total −0.778 −0.950* −0.554 Cu, Zn, Pb, Cd, Cr, and As concentrations of 16 urban − − − Cr-F1 0.775 0.952* 0.559 soils from five regions (utilities, commercial, industrial, − − − Cr-F2 0.763 0.956* 0.570 tourism, and roadside) of Lianyungang city were deter- − − − Cr-F3 0.816 0.922 0.549 mined. In this study, the mean levels of the six metals in − − − Cr-F4 0.750 0.962* 0.587 urban soils exceeded the coastal city soil background − − − Cr-F5 0.779 0.950 0.553 values of Jiangsu and China. Cu, Zn, Cd, and Cr had the * and ** indicated that the correlation was significant at the 0.05 highest levels in industrial areas, while Pb and As had and 0.01 levels, respectively the highest levels in roadside areas. These data suggest Environ Monit Assess (2017) 189:34 Page 11 of 13 34 that industrial emissions were major sources of Cu, Zn, Akan, J. C., Audu, S. 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