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Distribution of PAHs in tissues of wetland plants and the surrounding sediments in the Chongming wetland, Shanghai, China
Chemosphere 89 (2012) 221–227
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Distribution of PAHs in tissues of wetland plants and the surrounding sediments in the Chongming wetland, Shanghai, China Zucheng Wang a,b, Zhanfei Liu b, Yi Yang a, Tao Li a, Min Liu a,⇑ a b
Department of Geography, Key Laboratory of Geographic Information Science of the Ministry of Education, East China Normal University, Shanghai, China Marine Science Institute, The University of Texas at Austin, Port Aransas, TX, USA
a r t i c l e
i n f o
Article history: Received 3 January 2012 Received in revised form 8 April 2012 Accepted 9 April 2012 Available online 9 May 2012 Keywords: PAHs Wetland plants Sediment Plant tissues Chongming wetland RCF
a b s t r a c t Polycyclic aromatic hydrocarbons (PAHs) concentrations were determined in sediments and three types of wetland plants collected from the intertidal flats in the Chongming wetland. The concentration of total PAHs in sediments ranged from 38.7 to 136.2 ng g 1. Surface sediment concentrations were higher in regions with plant cover than in bare regions. Rhizome-layer sediments (56.8–102.4 ng g 1) contained less PAHs than surface sediments (0–5 cm). Concentrations of PAHs in plant tissues ranged from 51.9 to 181.2 ng g 1, with highest concentrations in the leaves of Scirpus. Most of the PAHs in the leaves and other plant tissues were low molecular weight compounds (LMW, 2–4 rings), and a similar distribution pattern of PAHs in different types of plants was also observed. Source analysis indicated that plants and sediments both came from pyrogenic sources, but plants had additional petroleum contamination. The low ratio of benzo[a]anthracene over chrysene suggests that the wetland PAHs came mainly from long-distance atmospheric transportation. Significant bioaccumulation of PAHs from the sediments into plants was not observed for high molecular weight PAHs (HMW, 5–6 rings) in Chongming wetland. The small RCFs (root concentration factor from sediments) for HMW PAHs and large RCFs for LMW PAHs suggested that roots accumulated LMW PAHs selectively from sediments in Chongming wetland. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Polycyclic aromatic hydrocarbons (PAHs), produced from incomplete combustion of organic materials and fossil fuel or directly sourced from petroleum, are distributed widely in natural environments. PAHs are one major type of persistent organic pollutants (POPs) with carcinogenic and mutagenic properties, and are resistant to biodegradation (Tremolada et al., 1996). PAHs can be introduced into ecosystems through plants, as leaves can take up PAHs from dry deposition or atmospheric gas forms (Simonich and Hites, 1994, 1995; Howsam et al., 2001; Barber et al., 2002; Moeckel et al., 2008), and roots may also take up PAHs from soil (O’Connor, 1996; Tam et al., 1996; Ryan et al., 1988; Gao and Zhu, 2004). Once PAHs penetrate into plant tissues, they can migrate from roots to leaves and vice versa (Korte et al., 2000). Some researchers conclude that PAHs are stored in plants through associations with lipids. However, PAH sorption by plants roots was correlated with the contents of both lipid and carbohydrate in plant roots, and carbohydrate may play an important role due to its high content in plants (Gao and Zhu, 2004; Zhang and Zhu, 2009). Indeed, PAHs in plants may exist mainly in the carbohydrate matrix.
⇑ Corresponding author. Tel.: +86 21 62232117; fax: +86 21 54345007. E-mail address: [email protected] (M. Liu). 0045-6535/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.chemosphere.2012.04.019
Some studies suggest that PAHs are transferred to plants from the atmosphere by deposition or by uptake in the gas phase through stomata, and from soil by roots (Simonich and Hites, 1995). However, the main paths of PAH accumulation in plants is still in debate. Kipopoulou et al. (1999) pointed out that PAHs may be adsorbed only through the epidermis of roots in contact with soil particles because of their high lipophility and low solubility, but not through the inner root, suggesting the atmosphere as the main way for PAHs to be combined into plants. In contrast, some researchers report a direct relationship between PAH concentrations in soil and plants, suggesting that the soil-to-root transfer dominates the atmosphere-to-plant pathway (Fismes et al., 2002). For some higher plants, such as Pennisetum purpureum, from an oil exploration site in Nigeria, the PAHs of low molecular weight (2–4 aromatic rings, LMW) occurred in higher abundance because of their greater vapor pressure, water solubility and bioavailability, in contrast with less high-molecular-weight PAHs (5–6 aromatic rings, HMW) that were preferentially associated with soil organic matter (Jánská et al., 2006; Sojinu et al., 2010). To date, most research focused on farmland and forest plants, few investigations considered the distribution of PAHs in wetland plants and surrounding sediments. Previous studies indicated that pollutants are concentrated in the estuary wetland environment (Liu et al., 2008), so it is important to know if PAHs are accumulated in wetland plants. PAHs were absorbed by wetland plants
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under controlled experimental conditions (Zhang et al., 2010). In the laboratory, PAHs were added and mixed homogeneously in a short period, and the PAHs were either in solution phase or adsorbed onto solid surfaces by physical mechanisms, so the plants may absorb PAHs easily. However, the uptake of PAHs is more complicated under in situ conditions because of multiple sources and the long-term accumulation of PAHs in sediments. Few studies have investigated uptake and distribution of organic pollutants in different tissues of natural wetland plants. In previous work, we found that the root of Scirpus, one type of wetland plant in the study area, sorbed more dichlorodiphenyltrichloroethanes (DDTs) than hexachlorocyclohexanes (HCHs), especially during the dry season (Liu et al., 2006). The object of this study was to elaborate the source and distribution of PAHs in sediments and plants tissues, PAH behaviors between sediments and plants roots and the bioaccumulation of PAHs by these wetland plants in Chongming wetland. We believe that this study is the first to analyze PAHs in different tissues of natural wetland plants in the study area. Sediments and typical plants in high-, mid- and lowtidelands collected in the dry-season (January) were examined. A second objective was to define plants useful as a biomonitor and for potential phytoremediation in Chongming wetland. 2. Materials and methods
and five deuterated PAHs (D8-Nap, D10-Ace, D10-Phe, D12-Chr, D12Per) (Dr. Ehrenstorfer, Germany) were used as the internal standard. All organic solvents are HPLC grade (J&K, China). The procedure for the PAH extraction was modified from Liang et al. (2007). Briefly, 5 g of sediments or 2 g of plant tissues were extracted with accelerated solvent extraction (ASE300 from DIONEX, USA) using a mixture of acetone and dichloromethane (1:1 v/v). The extraction cells were heated to 100 °C until the pressure of 10 MPa was reached. The static time was 5 min, the flush volume was 60%, and the purge time was 90 s. The final volume of the extract was approximately 30–40 mL, which was further concentrated with n-hexane to about 1 mL by a rotary evaporator. The concentrated extracts were purified with a self-packed chromatographic column. The column was packed with alumina (4 g, 50–200 meshes, activated at 160 °C for 16 h , and partially deactivated with 10% water), silica (8 g, 100–200 meshes, activated at 160 °C for 16 h, and partially deactivated with 10% water), and topped with 1 g of anhydrous sodium sulfate (baked at 450 °C for 4 h). The sample in the column was purified with 15 mL hexane which was discarded. It was eluted with 70 mL dichloromethane/hexane (3:7, v/v), which were collected. Finally, the collected solution was reduced to 1 mL by a rotary evaporator and transferred to a 2 mL vial, preserved in a freezer at 18 °C until gas chromatography–mass spectrometry (GC/MS) analysis.
2.1. Study area 2.4. PAH analysis The Chongming wetland is located on the east beach of Chongming Island, Shanghai, covers an area of about 214.55 km2, and is the biggest and most mature tidal wetland of all the estuaries in China. The Chongming wetland joined the RAMSAR Convention in 2001, and became one of the National Nature Reserves in China. From the land to the sea, this wetland can be divided into three parts: high tidal flats dominated by Phragmites australis and Spartina alternifloras, middle tidal flats by Scirpus mariqueter, and low tidal flats without plant cover. This wetland is flushed daily by the semidiurnal tides, ranging from 2 m to 4 m and with a speed of 0.5 m s 1. Details of the studied area were described previously (Hou et al., 2008).
The GC was equipped with an HP-5 MS capillary column (30 m 0.25 mm i.d., film thickness 0.25 lm), with helium as the carrier gas at 1 mL min 1 flow, using selective ion monitoring (SIM) mode to detect PAHs. The scan ions ranged from 127 to 279 a.m.u., and dwell time per ion was 10 ms (Table A1). The oven temperature was held at 40 °C for 4 min, increased to 280 °C at a rate of 10 °C min 1 and held for 4 min, and increased to 300 °C at a rate of 10 °C min 1 and held at 5 min. The injector and detector temperatures were 250 °C and 280 °C, respectively. The injection volume was 1 lL in a splitless mode. All peaks of the studied PAHs were eluted between 5 min and 20 min.
2.2. Sample collection
2.5. Quality assurance/quality control (QA/QC)
Phragmites (PH), Spartina alterniflora (SP), Scirpus (SC), surface sediments with plants (PHS, SPS, SCS), sediments without plants (NPS), and rhizospheric sediments (PHRS, SPRS, SCRS) were taken from different tidal flats in Chongming wetland in January 2011. Sediments were freeze-dried and sieved through a brass sieve (20 meshes) before extraction. Sufficient plant tissues were obtained for chemical analysis and reference, including seeds, leaves, stems and roots. Samples were wrapped immediately in aluminum foil and divided into different sub-samples after they were rinsed thoroughly with deionized water. All tissue samples were immediately frozen and stored at < 20 °C until further analysis.
Method blanks were analyzed by the same procedure as the samples to determine any background contamination. No PAHs were detected for our method blank. Spiked blanks (standards spiked into solvent) and sample duplicates were routinely analyzed with field samples. The recoveries for 16 PAHs of the spiked blanks ranged from 60% to 140%. To determine the recoveries of the PAH in real samples, an internal standard was added to the sample prior to extraction. The recovery of the internal standards in real samples ranged from 79% to 102%. The other four internal standards were used for quantification. 2.6. Principal component analysis
2.3. Sample extraction and cleanup Sixteen priority PAHs listed by the US Environmental Protection Agency (EPA) were analyzed: naphthalene (Nap), acenaphthene (Ace), acenaphthylene (Acy), fluorene (Fl), phenanthrene (Phe), anthracene (An), fluoranthene (Flu), pyrene (Pyr), benzo[a]anthracene (BaA), chrysene (Chr), benzo[b]fluoranthene (BbF), benzo[k, j]fluoranthene (BkF), benzo[a]pyrene (BaP), indeno[1, 2, 3]pyrene (InP), dibenzo[a, h]anthracene (DBA), and benzo[ghi]perylene (BgP). BbF and BkF were calculated together as BbkF because their peaks overlapped. A standard mixture of 16 US EPA-priority PAHs
Principal component analysis (PCA) is a multivariate regression analysis that can examine compositional differences among samples (e.g., Yunker et al., 1996; Ingalls et al., 2006). PCA generally reduces the number of variables into two major principle components, PC1 and PC2, which can explain most of the variance in a data matrix. Using MATLAB, we applied PCA on the data matrix that included different plant tissues and sediments. Concentrations of each PAH were standardized by subtracting the means and dividing by the standard deviations before PCA.
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3. Results and discussion 3.1. PAHs in the sediments and whole plants Among the sediments without plant cover, concentration of PAHs in low tidal flats was the lowest (38.7 ng g 1), with highest concentration occurring in high flats (109.9 ng g 1). Another survey in November 2010 showed the same trend, with PAHs ranging from 33.2 to 246.4 ng g 1 in sediments without plants. Such a difference between high and low tidal flats may result from the concentration of sedimentary organic carbon, which accounted for 0.21% and 0.72% in sediments from low tidal flats and high tidal flats, respectively (Zhang, 2010). Mean values of different plant tissues including leaves, stems, and roots, total PAH concentrations in whole plants ranged from 75.9 to 146.3 ng g 1. These values were higher than those in sediments except for the low Spartina alterniflora values (75.9 ng g 1). Concentrations of PAHs in surface sediments (0–5 cm) were higher than those in the rhizospheric zone (Table A2). This pattern suggested that roots may absorb PAHs from sediments. It is also possible that the degradation of PAHs was more intensive in the rhizosphere, as demonstrated by previous studies (Joner et al., 2002; Ma et al., 2010). However, plants might reduce the degradation of PAHs in certain environments where nutrients are insufficient by competing for nutrients with bacteria (Hodge et al., 2000). Contaminant levels in surface sediments of high tidal flats with PH cover were higher than those without cover (Table A2). Plants may transfer semi-volatile PAHs to sediments through falling leaves (Collins et al., 2006; Nizzetto et al., 2006). Indeed, the PAHs in leaves and surface sediments were highly correlated (Table A4). LMW PAHs were abundant in both the plants and sediments, with highest concentrations in Phe and Flu (Fig. 1). Also, concentrations of LMW PAHs were higher in plants than in sediments especially for Phe. Root uptake and transport in the transpiration stream was the dominant pathway for the accumulation of Pyr and Phe in plants, and roots preferred to take up Pyr than Phe (Gao and Zhu, 2004). So if we assume that Pyr and Phe are taken up by plants in a similar manner from sediments, relatively constant ratios of Pyr and Phe between sediments and plants are expected. However, the Phe level was much higher in plants than that in sediments, different than Pyr, suggesting that there is an additional source for Phe besides uptake from sediments. Previous research showed that LMW PAHs, such as Phe, were more abundant in atmospheric particles, and concentrated in sediments and leaves through deposition (Kaupp and McLachlan, 1999). The deposition of semi-volatile organic compounds with log KOA (octanol air partition coefficient) less than 8.5 can be partitioned into plants by equilibrium (McLachlan, 1999). Uptake from the atmosphere was an important pathway for organic contaminants with log KOA > 6 and log KAW > 6 (KAW: dimensionless air–water partition coefficient) (Cousins and Mackay, 2001). Phe, as a semi-volatile compound, was enriched in the air (Yang et al., 2010). Due to exposure to air on a long time scale, the high tidal flats with Phragmites contained more abundant Phe than the middle flat. Consistently, higher Phe concentrations in plants than that in sediments suggest that the plants absorb the Phe mainly from the atmosphere. Less abundant PAHs occurred in Spartina alterniflora and adjacent sediments than in Phragmites. This pattern may suggest that the lower PAH contents of Spartina alterniflora resulted from the enhanced PAH degradation in its rhizospheric zone by concentrated bacteria, or from a low bioaccumulation capacity. Low PAH concentrations in Spartina alterniflora was reported previously (Watts et al., 2006). The removal and degradation of PAHs depend strongly on rhizospheric processes and may vary across plant species (Ma et al., 2010).
Fig. 1. Contents of PAHs in the sediments and total plants. PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus; PHS, SPS, SCS stand for surface sediments with Phragmites; Spartina alterniflora; and Scirpus, separately; PHRS, SPRS, SCRS stand for rhizospheric sediments of Phragmites, Spartina alterniflora, and Scirpus, separately; T-PH, T-SP, T-SC stand for whole PAHs calculated by average PAHs in each tissue in Phragmites, Spartina alterniflora, and Scirpus, separately.
3.2. PAHs in different tissues Concentrations of PAHs in plant tissues ranged from 51.9 to 181.2 ng g 1, with the highest values in leaves of scirpus and the lowest values in the stems of Spartina alterniflora (Table 1). This distribution pattern of PAHs in plant tissues was consistent with previous studies with PAHs or other types of POPs (Liu et al., 2006; Desalme et al., 2011), even though the exact mechanism for the distribution is not yet clear. As discussed above, plants can absorb PAHs from both sediments and air. Airborne particulate and gaseous PAHs were likely the sources of PAHs for cuticle and the inner tissues in leaves, respectively (Wang et al., 2008). PAH concentrations increased from root, stem, to leaves in phragmites
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Table 1 PAHs distribution in tissues of different plants (ng g
Nap Acy Ace Fl Phe An Flu Pyr BaA Chr BbkF BaP InP DBA BgP T-PAHs
1
, dry weight for sediments and plants. PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus).
Leaves-PH
Stem-PH
Root-PH
Leaves-SP
Stem-SP
Root-SP
Seeds-SC
Leaves-SC
Rhizome-SC
8.2 1.2 0.8 9.5 73.0 2.3 33.6 14.0 2.1 13.5 5.6 2.4 3.0 0.7 0.2 170.1
9.3 1.0 1.8 6.2 31.4 2.2 12.0 7.1 0.5 2.9 Nd Nd 0.8 Nd 0.1 75.2
9.0 0.7 1.0 4.8 28.1 1.6 13.7 8.9 1.1 4.1 2.8 1.2 1.6 0.5 0.1 79.1
9.4 0.8 1.2 6.1 32.4 1.5 13.6 6.9 0.8 7.0 3.1 2.0 1.4 Nd 0.1 86.2
12.5 0.6 1.7 3.1 16.1 0.9 6.8 4.0 0.5 3.0 0.4 1.7 0.7 Nd 0.0 51.9
10.4 0.7 1.8 6.7 33.2 2.1 13.3 8.3 1.7 4.2 2.5 1.7 1.9 1.0 0.1 89.6
4.7 0.5 0.7 6.4 36.1 1.8 18.9 10.4 1.9 5.8 3.3 2.0 2.1 0.6 0.2 95.3
19.1 1.1 1.7 12.0 63.6 3.4 33.4 16.8 3.7 11.6 5.9 4.2 3.7 1.0 0.3 181.2
16.1 1.2 1.2 11.6 60.2 2.1 32.4 14.2 2.4 11.4 4.2 2.3 2.4 0.7 0.2 162.6
and scirpus, but a different pattern occurred in Spartina alterniflora, which contained more PAHs in roots. The transportation of PAHs from roots to leaves is limited for Spartina alterniflora (Watts et al., 2006). No accumulation of PAHs occurred in the seeds of scirpus, perhaps due to some unknown mechanism excluding PAHs during the building of seed biomass. PAH distribution patterns were similar in different tissues (Fig. 2), with 3–4 ring PAHs as the dominant compounds, accounting for more than 80% of the total PAHs. The content of lipid and carbohydrates in roots may affect the PAH sorption (Zhang and Zhu, 2009). Overall, the similar distribution patterns of PAHs among plant tissues indicated that a common mechanism controlled the transport of different types of PAHs within the plant or that the PAHs in plants were from same sources. 3.3. The source of PAHs Different PAH sources can generate PAH isomers in certain ratios, and these ratios are often relatively constant during the transportation or transferring in environments due to the similar thermostability of isomer pairs (Yunker et al., 2002). The ratios of An to 178 (An and Phe) and Flu to 202 (Flu and Pyr) can help differentiate the sources of PAHs (Lee et al., 1982; Budzinski et al.,
1997). A ratio of An/178 greater than 0.1, indicated that PAHs came from incomplete combustion, and ratios smaller than 0.1 suggested sources of petroleum products. A ratio of Flu to 202 less than 0.4, PAHs may indicate an oil source, exceeding 0.5 from coal and biomass burning, and between 0.4 and 0.5 from incomplete combustion of oil products (Yunker et al., 2002). According to these criteria, the ratios of PAHs in the plants and sediments were separated into two groups in Fig. 3. The PAHs in plants were from both coal and biomass burning and petroleum contamination, while the PAHs in the sediments samples may have originated mostly from incomplete burning of coal and biomass. However, the source identification by these simple ratios can be complicated by some caveats, such as diesel oil, shale oil or certain crude oil with >0.1 An/178 ratio, and some crude oil samples have Flu/202 ratios >0.4 (Yunker et al., 2002). Thus, the identified contamination sources can be viewed only as potential rather than conclusive. PCA was used to semi-quantitatively describe the contribution of main PAH sources to help clarify the relationship of PAHs in the plants and the sediments (Simcik et al., 1999; Ingalls et al., 2006). The first principal component (PC1) explained 73% of the variance, and PC 2 explained 15% of the rest variance (Fig. 4). The samples were separated clearly into two groups along the PC1, the sediments and the plant tissues, except that rhizospheric
Fig. 2. Percentages of PAH components in different plant tissues. PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus.
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Fig. 3. Diagnostics for distinguishing contamination sources of PAHs. L-flat = Low flat; M-flat = Middle flat; H-flat = high flat; NPS = surface Sediments No Plants covered; PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus; PHS, SPS, SCS stand for surface sediments with Phragmites; Spartina alterniflora and Scirpus, separately; PHRS, SPRS, SCRS stand for rhizospheric sediments of Phragmites, Spartina alterniflora and Scirpus, separately.
Fig. 4. Principal component analysis (PCA) on PAHs in sediments and plant tissues from Chongming wetland. PC1 explained 73% of the variance of the data matrix, and PC2 15% of the rest. The sediments and plant tissues were clearly separated into two groups along the PC1.
sediment with Spartina alterniflora was grouped with plant tissues. The plant tissues were enriched in Nap, Ace, Flu, Phe and Acy, the components from emission of oil, coal and cook oven gas (Table A4). In contrast, the sediments were enriched in Pyr, Chr, BbkF, BaA, BaP, InP, and DBA, the components from diesel oil and coal burning. These patterns again suggested that the sources of PAHs are different for the plant tissues and sediments in Chongming wetland. PAHs can be transferred by the long-range atmospheric transportation, but particle-associated PAHs have different stabilities during the transport. For example, pyrogenic ones are diluted or/ and degraded during the long-distance transportation. The ratio of BaA and Chr can help estimate the transportation distance of the PAHs from the source (Mai et al., 2003). A ratio less than 1 suggests that the PAHs were transported from a long distance;
otherwise, PAHs are considered to result from local pollution. The values in the plants were all less than 0.4, especially in the leaves (Fig. A.1b), suggesting that the PAHs in the plants came from long distance pollution, not from the local sediments. Atmospheric suspended particles are the dominant carrier for transfer of PAHs. Thus the PAHs in wetland plants come from atmospheric sedimentation and or gaseous transfer processes. The ratio of LMW over HMW PAHs ((Phe + An + Fl + Py)/(BaA + Chr + BbkF + BaP + InP + DahP + BghiP)), all above 1, indicate that the PAHs in plants may have originated from petrogenic sources (Soclo et al., 2000). For the sediments (Fig. A.1a), the ratios of BaA/Chr in the study area were smaller (0.44–0.63). Pyrogenic sources are believed to be enriched in HMW, but the ratio of LMW and HMW was higher in Chongming wetland than in sediments of Huangpu River in Shanghai (Liu et al., 2008). These results indicate that the PAHs
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in the Chongming wetland came mainly from petrogenic sources, and were diluted or/and degraded during the long-distance transportation to the sediments. 3.4. Sediment-root bioaccumulation factors (RCFs) Even though the above evidence suggests that most PAHs in plants were derived from the atmosphere, uptake of PAHs from sediments cannot be ruled out. Multiple PAHs sources are important to PAH bioavailability in environments (Thorsen et al., 2004). The similar PAH distribution patterns among plant tissues suggested that plants select LMW PAHs with relatively high solubility, and that the HMW ones are associated strongly with black carbons, which are difficult to incorporate into cells (Accardi-Dey and Gschwend, 2002). The PAHs concentration in roots correlated positively with those in rhizosphere sediments (Table A4), indicating that the PAHs in the roots may have in part come from the rhizospheric sediments. We calculated the RCFs of PAHs from the rhizosphere sediments to plants. Leaves can absorb PAHs from air, as indicated by the observation that a small fraction of PAHs in roots came from leaves (Desalme et al., 2011). Both averaged RCFs of plants were above 1 in our study (Table 2), but RCFs varied for different PAHs. The RCFs of most LMW PAHs were above 1, while those of the HMW PAHs were all below 1. This result indicated again that the LMW PAHs were accumulated more easily into the plants than were the HMW ones. In other words, the HMW PAHs had low bioaccessibility. The RCF of each plant correlated negatively with the KOW of PAHs (Fig. 5), as observed previously (Kipopoulou et al., 1999), suggesting that the uptake of PAHs by roots is controlled by their KOW values. 4. Conclusion Sixteen PAHs in sediments and plants from Chongming wetland, including surface and rhizosphere sediments, tissues of leaves, stems and roots, were determined systematically. Surface sediments with plant cover contained more PAHs than those without, and PAHs in rhizosphere sediments were lower than in surface sediments. For plants, the highest concentrations of PAHs were found in the Scirpus mariqueter, and the lowest in the Spartina alterniflora. In the plant tissues, PAHs increased from roots, stems to leaves, except Spartina alterniflora . The most abundant PAHs in the plant and sediments had low molecular weights. More highmolecular-weight ones were found in the sediments than in plants. The concentrations of PAHs among plant tissues varied but their Table 2 Bioaccumulation factors (RCFs) of PAHs for plants as calculated from roots to rhizosphere sediments. PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus. PH-RCFs
SP-RCFs
SC-RCFs
Nap Acy Ace Fl Phe An Flu Pyr BaA Chr BbkF BaP InP DBA BgP
9.3 1.6 6.4 1.6 2.2 0.8 0.8 0.7 0.2 0.3 0.4 0.2 0.2 0.3 0.3
1.4 1.2 2.4 1.5 2.0 1.7 2.0 1.6 0.9 1.0 0.8 0.7 1.0 1.8 1.0
5.2 2.1 3.1 3.3 3.9 0.9 1.7 1.1 0.3 0.9 0.6 0.3 0.4 0.4 0.3
Average
1.7
1.4
1.6
Fig. 5. Relationships between RCF and KOW of PAHs. Both variables are logtransformed. RCF was calculated from roots to rhizosphere sediments, PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus.
compositions were similar, suggesting that the mechanisms controlling the distribution of PAHs in plants were similar. The ratios of Flu/202 and An/178 and PCA indicated that a mixture of coal burning and petroleum contamination were the major sources of PAHs to the plants, but that pyrogenic sources such as diesel and coal burning supplied most of the PAHs to sediments. The RCFs values indicate that some LMW PAHs bioaccumulated from sediments to plants, but the HMW PAHs did not bioaccumulate significantly due to their low bioaccessibility. Acknowledgments We thank two anonymous reviewers for their valuable comments. We also thank W.S. Gardner for help with polishing the English. This work was supported by the grants from the National Natural Science Foundation of China (Grant Nos.# 41130525 and
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40971268), the Doctoral Fund of Ministry of Education of China (Grant No.# 20090076110020), and by Texas Higher Education Coordinating Board to Z. Liu (THECB#01859). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.chemosphere. 2012.04.019. References Accardi-Dey, A.M., Gschwend, P.M., 2002. Assessing the combined roles of natural organic matter and black carbon as sorbents in sediments. Environ. Sci. Technol. 36 (1), 21–29. Barber, J.L., Thomas, G.O., et al., 2002. Air-side and plant-side resistances influence the uptake of airborne PCBs by evergreen plants. Environ. Sci. Technol. 36 (15), 3224–3229. Budzinski, H., Jones, I., et al., 1997. Evaluation of sediment contamination by polycyclic aromatic hydrocarbons in the Gironde estuary. Mar. Chem. 58, 85– 97. Collins, C., Fryer, M., et al., 2006. Plant uptake of non-ionic organic chemicals. Environ. Sci. Technol. 40, 45–52. Cousins, I.T., Mackay, D., 2001. Strategies for including vegetation compartments in multimedia models. Chemosphere 44 (4), 643–654. Desalme, D., Binet, P., et al., 2011. Atmospheric phenanthrene transfer and effects on two grassland species and their root symbionts: a microcosm study. Environ. Exp. Bot. 71, 146–151. Fismes, J., Perrin-Ganier, C., et al., 2002. Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soils. J. Environ. Qual. 31, 1649–1656. Gao, Y.Z., Zhu, L.H., 2004. Plant uptake, accumulation, and translocation of phenanthrene and pyrene in soils. Chemosphere 55 (9), 1169–1178. Hodge, A., Stewart, J., et al., 2000. Competition between roots and soil microorganisms for nutrients from nitrogen-rich patches of varying complexity. J. Ecol. 88, 150–164. Hou, L.J., Liu, M., et al., 2008. Influences of the macrophyte (Scirpus mariqueter) on phosphorous geochemical properties in the intertidal marsh of the Yangtze estuary. J. Geophys. Res. – Biogeosci. 113. Howsam, M., Jones, K.C., et al., 2001. PAHs associated with the leaves of three deciduous tree species. II: uptake during a growing season. Chemosphere 44 (2), 155–164. Ingalls, A.E., Liu, Z.F., et al., 2006. Seasonal trends in the pigment and amino acid compositions of sinking particles in biogenic CaCO3 and SiO2 dominated regions of the Pacific sector of the southern ocean along 170 degrees W. Deep-sea Res. I 53, 836–859. Jánská, M., Hajslová, J., et al., 2006. Polycyclic aromatic hydrocarbons in fruits and vegetables grown in the Czech Republic. B Environ. Contam. Toxicol. 77, 492– 499. Joner, E.J., Corgie, S., et al., 2002. Nutritional constraints to PAH degradation in a simulated rhizosphere. Soil Biol. Biochem. 34, 859–864. Kaupp, H., McLachlan, M.S., 1999. Atmospheric particle size distributions of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) and polycyclic aromatic hydrocarbons (PAHs) and their implications for wet and dry deposition. Atmos Environ. 33, 85–95. Kipopoulou, A.M. et al., 1999. Bioconcentration of PAHs in vegetables grown in an industrial area. Environ. Pollut. 106, 369–380. Korte, F., Kvesitadze, G., et al., 2000. Review: organic toxicants and plants. Ecotoxicol. Environ. Saf. 47, 1–26. Lee, M.L., Vassilaros, L.D., et al., 1982. Capillary column gas chromatography of environmental polycyclic aromatic compounds. J. Anal. Chem. – Engl. Tr. 11, 251–262. Liang, Y., Tse, M.F., et al., 2007. Distribution patterns of polycyclic aromatic hydrocarbons (PAHs) in the sediments and fish at Mai Po marshes nature reserve, Hong Kong. Water Res. 41, 1303–1311.
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Distribution of PAHs in tissues of wetland plants and the surrounding sediments in the Chongming wetland, Shanghai, China Zucheng Wang a,b, Zhanfei Liu b, Yi Yang a, Tao Li a, Min Liu a,⇑ a b
Department of Geography, Key Laboratory of Geographic Information Science of the Ministry of Education, East China Normal University, Shanghai, China Marine Science Institute, The University of Texas at Austin, Port Aransas, TX, USA
a r t i c l e
i n f o
Article history: Received 3 January 2012 Received in revised form 8 April 2012 Accepted 9 April 2012 Available online 9 May 2012 Keywords: PAHs Wetland plants Sediment Plant tissues Chongming wetland RCF
a b s t r a c t Polycyclic aromatic hydrocarbons (PAHs) concentrations were determined in sediments and three types of wetland plants collected from the intertidal flats in the Chongming wetland. The concentration of total PAHs in sediments ranged from 38.7 to 136.2 ng g 1. Surface sediment concentrations were higher in regions with plant cover than in bare regions. Rhizome-layer sediments (56.8–102.4 ng g 1) contained less PAHs than surface sediments (0–5 cm). Concentrations of PAHs in plant tissues ranged from 51.9 to 181.2 ng g 1, with highest concentrations in the leaves of Scirpus. Most of the PAHs in the leaves and other plant tissues were low molecular weight compounds (LMW, 2–4 rings), and a similar distribution pattern of PAHs in different types of plants was also observed. Source analysis indicated that plants and sediments both came from pyrogenic sources, but plants had additional petroleum contamination. The low ratio of benzo[a]anthracene over chrysene suggests that the wetland PAHs came mainly from long-distance atmospheric transportation. Significant bioaccumulation of PAHs from the sediments into plants was not observed for high molecular weight PAHs (HMW, 5–6 rings) in Chongming wetland. The small RCFs (root concentration factor from sediments) for HMW PAHs and large RCFs for LMW PAHs suggested that roots accumulated LMW PAHs selectively from sediments in Chongming wetland. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Polycyclic aromatic hydrocarbons (PAHs), produced from incomplete combustion of organic materials and fossil fuel or directly sourced from petroleum, are distributed widely in natural environments. PAHs are one major type of persistent organic pollutants (POPs) with carcinogenic and mutagenic properties, and are resistant to biodegradation (Tremolada et al., 1996). PAHs can be introduced into ecosystems through plants, as leaves can take up PAHs from dry deposition or atmospheric gas forms (Simonich and Hites, 1994, 1995; Howsam et al., 2001; Barber et al., 2002; Moeckel et al., 2008), and roots may also take up PAHs from soil (O’Connor, 1996; Tam et al., 1996; Ryan et al., 1988; Gao and Zhu, 2004). Once PAHs penetrate into plant tissues, they can migrate from roots to leaves and vice versa (Korte et al., 2000). Some researchers conclude that PAHs are stored in plants through associations with lipids. However, PAH sorption by plants roots was correlated with the contents of both lipid and carbohydrate in plant roots, and carbohydrate may play an important role due to its high content in plants (Gao and Zhu, 2004; Zhang and Zhu, 2009). Indeed, PAHs in plants may exist mainly in the carbohydrate matrix.
⇑ Corresponding author. Tel.: +86 21 62232117; fax: +86 21 54345007. E-mail address: [email protected] (M. Liu). 0045-6535/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.chemosphere.2012.04.019
Some studies suggest that PAHs are transferred to plants from the atmosphere by deposition or by uptake in the gas phase through stomata, and from soil by roots (Simonich and Hites, 1995). However, the main paths of PAH accumulation in plants is still in debate. Kipopoulou et al. (1999) pointed out that PAHs may be adsorbed only through the epidermis of roots in contact with soil particles because of their high lipophility and low solubility, but not through the inner root, suggesting the atmosphere as the main way for PAHs to be combined into plants. In contrast, some researchers report a direct relationship between PAH concentrations in soil and plants, suggesting that the soil-to-root transfer dominates the atmosphere-to-plant pathway (Fismes et al., 2002). For some higher plants, such as Pennisetum purpureum, from an oil exploration site in Nigeria, the PAHs of low molecular weight (2–4 aromatic rings, LMW) occurred in higher abundance because of their greater vapor pressure, water solubility and bioavailability, in contrast with less high-molecular-weight PAHs (5–6 aromatic rings, HMW) that were preferentially associated with soil organic matter (Jánská et al., 2006; Sojinu et al., 2010). To date, most research focused on farmland and forest plants, few investigations considered the distribution of PAHs in wetland plants and surrounding sediments. Previous studies indicated that pollutants are concentrated in the estuary wetland environment (Liu et al., 2008), so it is important to know if PAHs are accumulated in wetland plants. PAHs were absorbed by wetland plants
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under controlled experimental conditions (Zhang et al., 2010). In the laboratory, PAHs were added and mixed homogeneously in a short period, and the PAHs were either in solution phase or adsorbed onto solid surfaces by physical mechanisms, so the plants may absorb PAHs easily. However, the uptake of PAHs is more complicated under in situ conditions because of multiple sources and the long-term accumulation of PAHs in sediments. Few studies have investigated uptake and distribution of organic pollutants in different tissues of natural wetland plants. In previous work, we found that the root of Scirpus, one type of wetland plant in the study area, sorbed more dichlorodiphenyltrichloroethanes (DDTs) than hexachlorocyclohexanes (HCHs), especially during the dry season (Liu et al., 2006). The object of this study was to elaborate the source and distribution of PAHs in sediments and plants tissues, PAH behaviors between sediments and plants roots and the bioaccumulation of PAHs by these wetland plants in Chongming wetland. We believe that this study is the first to analyze PAHs in different tissues of natural wetland plants in the study area. Sediments and typical plants in high-, mid- and lowtidelands collected in the dry-season (January) were examined. A second objective was to define plants useful as a biomonitor and for potential phytoremediation in Chongming wetland. 2. Materials and methods
and five deuterated PAHs (D8-Nap, D10-Ace, D10-Phe, D12-Chr, D12Per) (Dr. Ehrenstorfer, Germany) were used as the internal standard. All organic solvents are HPLC grade (J&K, China). The procedure for the PAH extraction was modified from Liang et al. (2007). Briefly, 5 g of sediments or 2 g of plant tissues were extracted with accelerated solvent extraction (ASE300 from DIONEX, USA) using a mixture of acetone and dichloromethane (1:1 v/v). The extraction cells were heated to 100 °C until the pressure of 10 MPa was reached. The static time was 5 min, the flush volume was 60%, and the purge time was 90 s. The final volume of the extract was approximately 30–40 mL, which was further concentrated with n-hexane to about 1 mL by a rotary evaporator. The concentrated extracts were purified with a self-packed chromatographic column. The column was packed with alumina (4 g, 50–200 meshes, activated at 160 °C for 16 h , and partially deactivated with 10% water), silica (8 g, 100–200 meshes, activated at 160 °C for 16 h, and partially deactivated with 10% water), and topped with 1 g of anhydrous sodium sulfate (baked at 450 °C for 4 h). The sample in the column was purified with 15 mL hexane which was discarded. It was eluted with 70 mL dichloromethane/hexane (3:7, v/v), which were collected. Finally, the collected solution was reduced to 1 mL by a rotary evaporator and transferred to a 2 mL vial, preserved in a freezer at 18 °C until gas chromatography–mass spectrometry (GC/MS) analysis.
2.1. Study area 2.4. PAH analysis The Chongming wetland is located on the east beach of Chongming Island, Shanghai, covers an area of about 214.55 km2, and is the biggest and most mature tidal wetland of all the estuaries in China. The Chongming wetland joined the RAMSAR Convention in 2001, and became one of the National Nature Reserves in China. From the land to the sea, this wetland can be divided into three parts: high tidal flats dominated by Phragmites australis and Spartina alternifloras, middle tidal flats by Scirpus mariqueter, and low tidal flats without plant cover. This wetland is flushed daily by the semidiurnal tides, ranging from 2 m to 4 m and with a speed of 0.5 m s 1. Details of the studied area were described previously (Hou et al., 2008).
The GC was equipped with an HP-5 MS capillary column (30 m 0.25 mm i.d., film thickness 0.25 lm), with helium as the carrier gas at 1 mL min 1 flow, using selective ion monitoring (SIM) mode to detect PAHs. The scan ions ranged from 127 to 279 a.m.u., and dwell time per ion was 10 ms (Table A1). The oven temperature was held at 40 °C for 4 min, increased to 280 °C at a rate of 10 °C min 1 and held for 4 min, and increased to 300 °C at a rate of 10 °C min 1 and held at 5 min. The injector and detector temperatures were 250 °C and 280 °C, respectively. The injection volume was 1 lL in a splitless mode. All peaks of the studied PAHs were eluted between 5 min and 20 min.
2.2. Sample collection
2.5. Quality assurance/quality control (QA/QC)
Phragmites (PH), Spartina alterniflora (SP), Scirpus (SC), surface sediments with plants (PHS, SPS, SCS), sediments without plants (NPS), and rhizospheric sediments (PHRS, SPRS, SCRS) were taken from different tidal flats in Chongming wetland in January 2011. Sediments were freeze-dried and sieved through a brass sieve (20 meshes) before extraction. Sufficient plant tissues were obtained for chemical analysis and reference, including seeds, leaves, stems and roots. Samples were wrapped immediately in aluminum foil and divided into different sub-samples after they were rinsed thoroughly with deionized water. All tissue samples were immediately frozen and stored at < 20 °C until further analysis.
Method blanks were analyzed by the same procedure as the samples to determine any background contamination. No PAHs were detected for our method blank. Spiked blanks (standards spiked into solvent) and sample duplicates were routinely analyzed with field samples. The recoveries for 16 PAHs of the spiked blanks ranged from 60% to 140%. To determine the recoveries of the PAH in real samples, an internal standard was added to the sample prior to extraction. The recovery of the internal standards in real samples ranged from 79% to 102%. The other four internal standards were used for quantification. 2.6. Principal component analysis
2.3. Sample extraction and cleanup Sixteen priority PAHs listed by the US Environmental Protection Agency (EPA) were analyzed: naphthalene (Nap), acenaphthene (Ace), acenaphthylene (Acy), fluorene (Fl), phenanthrene (Phe), anthracene (An), fluoranthene (Flu), pyrene (Pyr), benzo[a]anthracene (BaA), chrysene (Chr), benzo[b]fluoranthene (BbF), benzo[k, j]fluoranthene (BkF), benzo[a]pyrene (BaP), indeno[1, 2, 3]pyrene (InP), dibenzo[a, h]anthracene (DBA), and benzo[ghi]perylene (BgP). BbF and BkF were calculated together as BbkF because their peaks overlapped. A standard mixture of 16 US EPA-priority PAHs
Principal component analysis (PCA) is a multivariate regression analysis that can examine compositional differences among samples (e.g., Yunker et al., 1996; Ingalls et al., 2006). PCA generally reduces the number of variables into two major principle components, PC1 and PC2, which can explain most of the variance in a data matrix. Using MATLAB, we applied PCA on the data matrix that included different plant tissues and sediments. Concentrations of each PAH were standardized by subtracting the means and dividing by the standard deviations before PCA.
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3. Results and discussion 3.1. PAHs in the sediments and whole plants Among the sediments without plant cover, concentration of PAHs in low tidal flats was the lowest (38.7 ng g 1), with highest concentration occurring in high flats (109.9 ng g 1). Another survey in November 2010 showed the same trend, with PAHs ranging from 33.2 to 246.4 ng g 1 in sediments without plants. Such a difference between high and low tidal flats may result from the concentration of sedimentary organic carbon, which accounted for 0.21% and 0.72% in sediments from low tidal flats and high tidal flats, respectively (Zhang, 2010). Mean values of different plant tissues including leaves, stems, and roots, total PAH concentrations in whole plants ranged from 75.9 to 146.3 ng g 1. These values were higher than those in sediments except for the low Spartina alterniflora values (75.9 ng g 1). Concentrations of PAHs in surface sediments (0–5 cm) were higher than those in the rhizospheric zone (Table A2). This pattern suggested that roots may absorb PAHs from sediments. It is also possible that the degradation of PAHs was more intensive in the rhizosphere, as demonstrated by previous studies (Joner et al., 2002; Ma et al., 2010). However, plants might reduce the degradation of PAHs in certain environments where nutrients are insufficient by competing for nutrients with bacteria (Hodge et al., 2000). Contaminant levels in surface sediments of high tidal flats with PH cover were higher than those without cover (Table A2). Plants may transfer semi-volatile PAHs to sediments through falling leaves (Collins et al., 2006; Nizzetto et al., 2006). Indeed, the PAHs in leaves and surface sediments were highly correlated (Table A4). LMW PAHs were abundant in both the plants and sediments, with highest concentrations in Phe and Flu (Fig. 1). Also, concentrations of LMW PAHs were higher in plants than in sediments especially for Phe. Root uptake and transport in the transpiration stream was the dominant pathway for the accumulation of Pyr and Phe in plants, and roots preferred to take up Pyr than Phe (Gao and Zhu, 2004). So if we assume that Pyr and Phe are taken up by plants in a similar manner from sediments, relatively constant ratios of Pyr and Phe between sediments and plants are expected. However, the Phe level was much higher in plants than that in sediments, different than Pyr, suggesting that there is an additional source for Phe besides uptake from sediments. Previous research showed that LMW PAHs, such as Phe, were more abundant in atmospheric particles, and concentrated in sediments and leaves through deposition (Kaupp and McLachlan, 1999). The deposition of semi-volatile organic compounds with log KOA (octanol air partition coefficient) less than 8.5 can be partitioned into plants by equilibrium (McLachlan, 1999). Uptake from the atmosphere was an important pathway for organic contaminants with log KOA > 6 and log KAW > 6 (KAW: dimensionless air–water partition coefficient) (Cousins and Mackay, 2001). Phe, as a semi-volatile compound, was enriched in the air (Yang et al., 2010). Due to exposure to air on a long time scale, the high tidal flats with Phragmites contained more abundant Phe than the middle flat. Consistently, higher Phe concentrations in plants than that in sediments suggest that the plants absorb the Phe mainly from the atmosphere. Less abundant PAHs occurred in Spartina alterniflora and adjacent sediments than in Phragmites. This pattern may suggest that the lower PAH contents of Spartina alterniflora resulted from the enhanced PAH degradation in its rhizospheric zone by concentrated bacteria, or from a low bioaccumulation capacity. Low PAH concentrations in Spartina alterniflora was reported previously (Watts et al., 2006). The removal and degradation of PAHs depend strongly on rhizospheric processes and may vary across plant species (Ma et al., 2010).
Fig. 1. Contents of PAHs in the sediments and total plants. PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus; PHS, SPS, SCS stand for surface sediments with Phragmites; Spartina alterniflora; and Scirpus, separately; PHRS, SPRS, SCRS stand for rhizospheric sediments of Phragmites, Spartina alterniflora, and Scirpus, separately; T-PH, T-SP, T-SC stand for whole PAHs calculated by average PAHs in each tissue in Phragmites, Spartina alterniflora, and Scirpus, separately.
3.2. PAHs in different tissues Concentrations of PAHs in plant tissues ranged from 51.9 to 181.2 ng g 1, with the highest values in leaves of scirpus and the lowest values in the stems of Spartina alterniflora (Table 1). This distribution pattern of PAHs in plant tissues was consistent with previous studies with PAHs or other types of POPs (Liu et al., 2006; Desalme et al., 2011), even though the exact mechanism for the distribution is not yet clear. As discussed above, plants can absorb PAHs from both sediments and air. Airborne particulate and gaseous PAHs were likely the sources of PAHs for cuticle and the inner tissues in leaves, respectively (Wang et al., 2008). PAH concentrations increased from root, stem, to leaves in phragmites
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Table 1 PAHs distribution in tissues of different plants (ng g
Nap Acy Ace Fl Phe An Flu Pyr BaA Chr BbkF BaP InP DBA BgP T-PAHs
1
, dry weight for sediments and plants. PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus).
Leaves-PH
Stem-PH
Root-PH
Leaves-SP
Stem-SP
Root-SP
Seeds-SC
Leaves-SC
Rhizome-SC
8.2 1.2 0.8 9.5 73.0 2.3 33.6 14.0 2.1 13.5 5.6 2.4 3.0 0.7 0.2 170.1
9.3 1.0 1.8 6.2 31.4 2.2 12.0 7.1 0.5 2.9 Nd Nd 0.8 Nd 0.1 75.2
9.0 0.7 1.0 4.8 28.1 1.6 13.7 8.9 1.1 4.1 2.8 1.2 1.6 0.5 0.1 79.1
9.4 0.8 1.2 6.1 32.4 1.5 13.6 6.9 0.8 7.0 3.1 2.0 1.4 Nd 0.1 86.2
12.5 0.6 1.7 3.1 16.1 0.9 6.8 4.0 0.5 3.0 0.4 1.7 0.7 Nd 0.0 51.9
10.4 0.7 1.8 6.7 33.2 2.1 13.3 8.3 1.7 4.2 2.5 1.7 1.9 1.0 0.1 89.6
4.7 0.5 0.7 6.4 36.1 1.8 18.9 10.4 1.9 5.8 3.3 2.0 2.1 0.6 0.2 95.3
19.1 1.1 1.7 12.0 63.6 3.4 33.4 16.8 3.7 11.6 5.9 4.2 3.7 1.0 0.3 181.2
16.1 1.2 1.2 11.6 60.2 2.1 32.4 14.2 2.4 11.4 4.2 2.3 2.4 0.7 0.2 162.6
and scirpus, but a different pattern occurred in Spartina alterniflora, which contained more PAHs in roots. The transportation of PAHs from roots to leaves is limited for Spartina alterniflora (Watts et al., 2006). No accumulation of PAHs occurred in the seeds of scirpus, perhaps due to some unknown mechanism excluding PAHs during the building of seed biomass. PAH distribution patterns were similar in different tissues (Fig. 2), with 3–4 ring PAHs as the dominant compounds, accounting for more than 80% of the total PAHs. The content of lipid and carbohydrates in roots may affect the PAH sorption (Zhang and Zhu, 2009). Overall, the similar distribution patterns of PAHs among plant tissues indicated that a common mechanism controlled the transport of different types of PAHs within the plant or that the PAHs in plants were from same sources. 3.3. The source of PAHs Different PAH sources can generate PAH isomers in certain ratios, and these ratios are often relatively constant during the transportation or transferring in environments due to the similar thermostability of isomer pairs (Yunker et al., 2002). The ratios of An to 178 (An and Phe) and Flu to 202 (Flu and Pyr) can help differentiate the sources of PAHs (Lee et al., 1982; Budzinski et al.,
1997). A ratio of An/178 greater than 0.1, indicated that PAHs came from incomplete combustion, and ratios smaller than 0.1 suggested sources of petroleum products. A ratio of Flu to 202 less than 0.4, PAHs may indicate an oil source, exceeding 0.5 from coal and biomass burning, and between 0.4 and 0.5 from incomplete combustion of oil products (Yunker et al., 2002). According to these criteria, the ratios of PAHs in the plants and sediments were separated into two groups in Fig. 3. The PAHs in plants were from both coal and biomass burning and petroleum contamination, while the PAHs in the sediments samples may have originated mostly from incomplete burning of coal and biomass. However, the source identification by these simple ratios can be complicated by some caveats, such as diesel oil, shale oil or certain crude oil with >0.1 An/178 ratio, and some crude oil samples have Flu/202 ratios >0.4 (Yunker et al., 2002). Thus, the identified contamination sources can be viewed only as potential rather than conclusive. PCA was used to semi-quantitatively describe the contribution of main PAH sources to help clarify the relationship of PAHs in the plants and the sediments (Simcik et al., 1999; Ingalls et al., 2006). The first principal component (PC1) explained 73% of the variance, and PC 2 explained 15% of the rest variance (Fig. 4). The samples were separated clearly into two groups along the PC1, the sediments and the plant tissues, except that rhizospheric
Fig. 2. Percentages of PAH components in different plant tissues. PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus.
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Fig. 3. Diagnostics for distinguishing contamination sources of PAHs. L-flat = Low flat; M-flat = Middle flat; H-flat = high flat; NPS = surface Sediments No Plants covered; PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus; PHS, SPS, SCS stand for surface sediments with Phragmites; Spartina alterniflora and Scirpus, separately; PHRS, SPRS, SCRS stand for rhizospheric sediments of Phragmites, Spartina alterniflora and Scirpus, separately.
Fig. 4. Principal component analysis (PCA) on PAHs in sediments and plant tissues from Chongming wetland. PC1 explained 73% of the variance of the data matrix, and PC2 15% of the rest. The sediments and plant tissues were clearly separated into two groups along the PC1.
sediment with Spartina alterniflora was grouped with plant tissues. The plant tissues were enriched in Nap, Ace, Flu, Phe and Acy, the components from emission of oil, coal and cook oven gas (Table A4). In contrast, the sediments were enriched in Pyr, Chr, BbkF, BaA, BaP, InP, and DBA, the components from diesel oil and coal burning. These patterns again suggested that the sources of PAHs are different for the plant tissues and sediments in Chongming wetland. PAHs can be transferred by the long-range atmospheric transportation, but particle-associated PAHs have different stabilities during the transport. For example, pyrogenic ones are diluted or/ and degraded during the long-distance transportation. The ratio of BaA and Chr can help estimate the transportation distance of the PAHs from the source (Mai et al., 2003). A ratio less than 1 suggests that the PAHs were transported from a long distance;
otherwise, PAHs are considered to result from local pollution. The values in the plants were all less than 0.4, especially in the leaves (Fig. A.1b), suggesting that the PAHs in the plants came from long distance pollution, not from the local sediments. Atmospheric suspended particles are the dominant carrier for transfer of PAHs. Thus the PAHs in wetland plants come from atmospheric sedimentation and or gaseous transfer processes. The ratio of LMW over HMW PAHs ((Phe + An + Fl + Py)/(BaA + Chr + BbkF + BaP + InP + DahP + BghiP)), all above 1, indicate that the PAHs in plants may have originated from petrogenic sources (Soclo et al., 2000). For the sediments (Fig. A.1a), the ratios of BaA/Chr in the study area were smaller (0.44–0.63). Pyrogenic sources are believed to be enriched in HMW, but the ratio of LMW and HMW was higher in Chongming wetland than in sediments of Huangpu River in Shanghai (Liu et al., 2008). These results indicate that the PAHs
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in the Chongming wetland came mainly from petrogenic sources, and were diluted or/and degraded during the long-distance transportation to the sediments. 3.4. Sediment-root bioaccumulation factors (RCFs) Even though the above evidence suggests that most PAHs in plants were derived from the atmosphere, uptake of PAHs from sediments cannot be ruled out. Multiple PAHs sources are important to PAH bioavailability in environments (Thorsen et al., 2004). The similar PAH distribution patterns among plant tissues suggested that plants select LMW PAHs with relatively high solubility, and that the HMW ones are associated strongly with black carbons, which are difficult to incorporate into cells (Accardi-Dey and Gschwend, 2002). The PAHs concentration in roots correlated positively with those in rhizosphere sediments (Table A4), indicating that the PAHs in the roots may have in part come from the rhizospheric sediments. We calculated the RCFs of PAHs from the rhizosphere sediments to plants. Leaves can absorb PAHs from air, as indicated by the observation that a small fraction of PAHs in roots came from leaves (Desalme et al., 2011). Both averaged RCFs of plants were above 1 in our study (Table 2), but RCFs varied for different PAHs. The RCFs of most LMW PAHs were above 1, while those of the HMW PAHs were all below 1. This result indicated again that the LMW PAHs were accumulated more easily into the plants than were the HMW ones. In other words, the HMW PAHs had low bioaccessibility. The RCF of each plant correlated negatively with the KOW of PAHs (Fig. 5), as observed previously (Kipopoulou et al., 1999), suggesting that the uptake of PAHs by roots is controlled by their KOW values. 4. Conclusion Sixteen PAHs in sediments and plants from Chongming wetland, including surface and rhizosphere sediments, tissues of leaves, stems and roots, were determined systematically. Surface sediments with plant cover contained more PAHs than those without, and PAHs in rhizosphere sediments were lower than in surface sediments. For plants, the highest concentrations of PAHs were found in the Scirpus mariqueter, and the lowest in the Spartina alterniflora. In the plant tissues, PAHs increased from roots, stems to leaves, except Spartina alterniflora . The most abundant PAHs in the plant and sediments had low molecular weights. More highmolecular-weight ones were found in the sediments than in plants. The concentrations of PAHs among plant tissues varied but their Table 2 Bioaccumulation factors (RCFs) of PAHs for plants as calculated from roots to rhizosphere sediments. PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus. PH-RCFs
SP-RCFs
SC-RCFs
Nap Acy Ace Fl Phe An Flu Pyr BaA Chr BbkF BaP InP DBA BgP
9.3 1.6 6.4 1.6 2.2 0.8 0.8 0.7 0.2 0.3 0.4 0.2 0.2 0.3 0.3
1.4 1.2 2.4 1.5 2.0 1.7 2.0 1.6 0.9 1.0 0.8 0.7 1.0 1.8 1.0
5.2 2.1 3.1 3.3 3.9 0.9 1.7 1.1 0.3 0.9 0.6 0.3 0.4 0.4 0.3
Average
1.7
1.4
1.6
Fig. 5. Relationships between RCF and KOW of PAHs. Both variables are logtransformed. RCF was calculated from roots to rhizosphere sediments, PH = Phragmites; SP = Spartina alterniflora; SC = Scirpus.
compositions were similar, suggesting that the mechanisms controlling the distribution of PAHs in plants were similar. The ratios of Flu/202 and An/178 and PCA indicated that a mixture of coal burning and petroleum contamination were the major sources of PAHs to the plants, but that pyrogenic sources such as diesel and coal burning supplied most of the PAHs to sediments. The RCFs values indicate that some LMW PAHs bioaccumulated from sediments to plants, but the HMW PAHs did not bioaccumulate significantly due to their low bioaccessibility. Acknowledgments We thank two anonymous reviewers for their valuable comments. We also thank W.S. Gardner for help with polishing the English. This work was supported by the grants from the National Natural Science Foundation of China (Grant Nos.# 41130525 and
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