Reduced bioavailability and ecological risks of polycyclic aromatic hydrocarbons in Yangshan port of East China Sea: Remediation effectiveness in the transition from construction to operation

Science of the Total Environment 687 (2019) 679–686

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Reduced bioavailability and ecological risks of polycyclic aromatic hydrocarbons in Yangshan port of East China Sea: Remediation effectiveness in the transition from construction to operation Juan-Ying Li a, Wenjian Yu a, Jie Yin a, Yiqin Chen a, Qian Wang a, Ling Jin b,⁎ a b

College of Marine Ecology and Environment, Shanghai Ocean University, Shanghai 201306, China Department of Civil and Environmental Engineering, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Equilibrium sampling senses freelydissolved concentrations and fluxes of PAHs • Trophic magnification present in the pelagic food web but not in the benthic one • Higher burden of PAHs in benthic species due to habitat-specific bioavailability • Reduced risks due to lowered bioavailability and bioaccumulation of PAHs • Remediation effectiveness of PAHs from construction to operation in Yangshan Port

a r t i c l e

i n f o

Article history: Received 31 December 2018 Received in revised form 3 June 2019 Accepted 3 June 2019 Available online 4 June 2019 Editor: Filip M.G. Tack Keywords: Marine pollution Bioavailability Equilibrium sampling Thermodynamic potential Ecological risk

⁎ Corresponding author. E-mail address: [email protected] (L. Jin).

https://doi.org/10.1016/j.scitotenv.2019.06.040 0048-9697/© 2019 Elsevier B.V. All rights reserved.

a b s t r a c t To assess the remediation effectiveness of ecological restoration in the transition period from construction to operation of Yangshan Port, the largest deepwater port of East China Sea, we employed equilibrium passive sampling and partitioning theory to assess the changing bioavailability and flux of polycyclic aromatic hydrocarbons (PAHs) in relation to bioaccumulation and ecological risks in marine organisms. Due to the ecological restoration efforts, both the bulk and bioavailable concentrations of PAHs in sediment and surface seawater samples decreased dramatically after the port entered the operation phase, as compared with those reported during the last construction phase. PAH concentrations in the marine organisms also showed a dramatic decline, and corresponded to the change in the freely dissolved fractions of PAHs in sediment/surface water according to their thermodynamic potential for bioaccumulation. While trophic magnification of ΣPAHs was observed in the pelagic communities, concentrations of PAHs in benthic species were relatively consistent across multiple trophic levels, and were generally higher than those in pelagic species. The differing bioaccumulation between benthic and pelagic species may be related to the habitat-specific bioavailability of PAHs and the prey-predator relations among different species. The incremental lifetime cancer risks (ILCR) of PAHs in marine organisms also dropped by nearly three orders of magnitude, and were lower than the guideline (1 × 10−6) proposed by the U.S. EPA, except for several species at higher trophic levels. Overall, our study highlights an integrated use of passive sampling and equilibrium partitioning theory as a robust tool that can be applied to assess the effectiveness of ecological remediation in the port environment with quantitative, mechanistic insights from bioavailability to bioaccumulation. © 2019 Elsevier B.V. All rights reserved.

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1. Introduction Many of the world's great cities are located on the coast with working ports and harbours that are part of the fundamental fabric of those communities. This is also true to Shanghai, a coastal metropolis of China, with Yangshan Port, the largest deepwater port of East China Sea. Built on the offshore islands in the Yangtze River Estuary, the port experienced four stages of construction between 2001 and 2015, resulting in a total of 30 berths capable of handling 15 million TEUs annually. Environmental degradation and ecosystem restoration are key issues surrounding port development in balance with a sustainable marine environment. Port waters and sediments often become enriched with nutrients and subject to elevated loads of pollutants, such as heavy metals and organic contaminants, including petroleum- and combustion-derived polycyclic aromatic hydrocarbons (PAHs). PAHs, mainly from the combustion of fossil fuels and the direct release of crude oil and related products (Simpson et al., 1996), have aroused widespread public concern due to their mutagenicity, carcinogenicity and persistence. Our earlier investigation in Yangshan Port (Li et al., 2015b) revealed that large-scale and extensive port-related constructions led to a ubiquitous contamination of petroleum- and combustion-derived PAHs in the port waters. Particularly, maritime transport related activities, such as crude oil spillage and leakage, vessel sewage, ballast water discharge and combustion of fossil fuels, were the major sources of PAHs in harbor or port waters (Li et al., 2015c; Parinos and Gogou, 2016; PérezFernández et al., 2015; Ruiz-Fernández et al., 2016; Varnosfaderany et al., 2014; Burns, 2014; Xue et al., 2016). The ∑PAHs concentrations (1100–29,000 ng/g dw) in one of the benthic organisms, oysters (S. cucullata), collected from the port area were ranked at the highest end of the global reported concentration range. It is known that coastal organisms, including pelagic and benthic species, can accumulate high levels of PAHs from seawater through respiration and daily diet input (Samuelsson et al., 2015; Kim et al., 2014; Casado-Martinez et al., 2008; Lacroix et al., 2015). High residues of PAHs in marine organisms and trophic transfer along the food chain may cause adverse effects on the marine ecosystem, as well as pose potential threats to coastal residents who consume a large amount of seafood (Nasher et al., 2016). Up to 2016, the large-scale construction in Yangshan Port was completed and the port entered the operation phase. During this transition period, a number of projects were undertaken in the port area, including some measures to control pollutant emissions, such as (1) sediment dredging to deepen navigation channel and remove contaminants in surface sediments from precipitation of suspended solids in overlaying seawater; (2) pollutant reduction from surface runoff via soil improvement, slope flexible protection system, and rock side slope vertical greening technology; (3) point source controls; and (4) ecological remediation measures, including artificial reef deployment along the coastal area to restore the seabed environment (Wang et al., 2015), wetland phytoremediation in the peripheral waters of the port (i.e. largescale cultivation of Scirpus mariqueter Tang et Wang) to remove the dominant low molecular weight PAHs due to the large storage capacity of macrophytes for less hydrophobic compounds (Kong et al., 2017), and implementation of closed fishing seasons and bottom trawling ban in the port area. While all the above measures taken were meant to reduce the concentrations of contaminants in seawater and sediments in order for reduced bioaccumulation potentials of these compounds in marine organisms and better environmental safety of the port ecosystem. However, the effectiveness of the ecological remediation is yet to be assessed. The traditional method for assessing remediation is to compare the bulk concentrations of contaminants in different matrices before and after remediation. However, it is difficult to reflect the changes in chemical activity or bioavailability of contaminants. Information regarding the bioavailability of organic chemicals is important in evaluating the ecological remediation and determining the bioaccumulation potentials

of these contaminants in marine organisms (Ramdine et al., 2012). The bioavailability of hydrophobic organic contaminants (HOCs) can be assessed by their freely dissolved concentration (Cfree) in overlying water or sediment pore water (Mayer et al., 2000; Mayer et al., 2014; Jager et al., 2003; Li et al., 2016; Li et al., 2018), as Cfree is a central mediator driving the bioaccumulation process from water or sediment to the exposed aquatic organisms. The equilibrium sampling technique using polymers (e.g., polydimethylsiloxane or PDMS) has been established to measure Cfree of chemicals via PDMS-water partition coefficients (KPDMSw) (Hunter et al., 2008; Mayer et al., 2014). PDMS, as a biomimetic tool, has been widely used to predict the bioaccumulation potential of chemicals in sediment-dwelling organisms and been considered as a benchmark of bioavailability of sediment-associated contaminants when equilibrium of chemicals between sediment pore water and PDMS is achieved (Lang et al., 2015; Li et al., 2015a; Thomas et al., 2014). Lipid-based tissue concentrations in many kinds of aquatic organisms from lakes, rivers, and oceans can be predicted by the thermodynamic potential calculation with Cfree sensed by passive sampling (Tuikka et al., 2016; Figueiredo et al., 2017; Thomas et al., 2014). Quantitative conversion of Cfree into tissue residues in benthic organisms as well as total chemical burden in sediment was also demonstrated in recent studies for PAHs in freshwater (Li et al., 2016) and pyrethroid pesticides in mariculture systems (Li et al., 2018). The bioavailability and flux of PAHs based on chemical activity and their impacts on bioaccumulation potentials of PAHs in marine organisms from adjacent waters after ecological remediation were rarely reported in Yangshan Port. It is imperative to understand the changing flux and bioavailability of PAHs in the port waters in a predictive linkage with their bioaccumulation potentials in marine organisms and trophic transfer through the food chain before and after ecological remediation. This will provide scientific guidance for ecological remediation and risk mitigation in contaminated areas affected by port activities. To this end, in the current study, equilibrium sampling based on the PDMS polymer was used to assess the changing bioavailability and flux of PAHs at the sediment-water interface with predictive links to trophic accumulation and ecological risks of PAHs in the marine organisms. We aimed to evaluate the effectiveness of the ecological remediation projects in the transition period of the port from construction to operation. 2. Materials and methods 2.1. Sample collection Seventeen sampling sites (S1–S17) were selected in Yangshan Port (Fig. 1). Samples of surface seawater and sediment were collected from S1 to S8. These sites were consistent with those in the construction period reported previously by Li et al. (2015a). The benthic organisms were also collected from S1 to S8, however, pelagic organisms were collected from S9 to S17. Sampling was performed three times in May, July and September, respectively. Samples of surface seawater were stored in clean glass bottles and analyzed within 24 h after they were transported to laboratory in an ice box. Surface sediments (0–5 cm) from intertidal zone were collected using a petite ponar grab and stored in aluminum cans. Eight benthic species were collected from intertidal zone at low tide and 11 pelagic species were collected by trawl. The foraging habitats and behavior of these animals were summarized in Table S1. All biota samples were wrapped in aluminum foil. Both sediments and biota samples were transported to laboratory in an icebox and stored at −20 °C until analysis. 2.2. Sample preparation and lipid content measurement PAHs were extracted from all samples including surface seawater, surface sediment, and marine organisms. The extraction methods followed previously established procedure (Li et al., 2015b). Briefly, for seawater, 5 g of NaCl and 10 mL methanol were added to the filtered

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Fig. 1. Sampling sites in Yangshan Port.

water sample (1 L, 0.45 μm hybrid fiber membrane, Bandao, China). PAHs were enriched by the solid phase extraction using C18 cartridge (Supelclean, China) at a flow rate of 8 mL/min and eluted by 15 mL of dichloromethane. Finally, the extracts were concentrated to 1 mL under a gentle stream of nitrogen. For sediment, 2 g of freeze-dried sample, with activated copper mixed for desulfurization, was extracted on Soxhlet using a solvent mixture of hexane and acetone (1:1, V/V) at 65 °C for 24 h. The extracts were collected and condensed to 10 mL on a rotary evaporator. The extracts were then loaded onto a silica gel column for cleanup, and eluted by 45 mL of n-hexane/dichloromethane (3:7, V/V) twice. Finally, the eluate was combined and reduced to 1 mL under a gentle stream of nitrogen for instrumental analysis. Muscle tissues of larger species, such as fish, were used for chemical analysis, while the whole body of smaller species, such as shrimps, was used. Freeze-dried tissue samples (~2 g) were extracted on Soxhlet at 65 °C for 24 h with a solvent mixture of hexane and acetone (1:1, V/V). The extracts were concentrated to approximately 10 mL on a rotary evaporator and passed through a Florisil column. The column was eluted by 20 mL of dichloromethane to retrieve the PAHs. Extracts were finally reduced to 1 mL under a gentle stream of nitrogen for instrumental analysis. Three replicates were prepared for each sample, including surface seawater, surface sediments, and marine organisms. Lipid contents of marine organisms were measured according to the extraction methods described by Li et al. (2018). Five subsamples were used for the lipid content determination for each species, and the mean value (based on tissue dry weight) was used and shown in Table S1.

2.3. Bioavailability assessment of sediment-associated PAHs Medical grade coated polydimethylsiloxane (PDMS) sheet (density of 0.97 g/mL, Specialty Silicone Products Inc., Ballston Spa, NY) was used to measure the Cfree of PAHs to estimate the bioavailability of sediment-associated PAHs following the method established previously (Li et al., 2013). Briefly, PDMS was sonicated with hexane and methanol (1:1, V/V) for 15 min before use. One piece of PDMS and wet sediment (approximately 60% water content) were placed into a clean amber glass jar. A blank jar containing ultra-pure water served as a laboratory blank. HgCl2 (0.15% of sediment dry weight) was added to each jar to hinder biological activity and stabilize the sample during the experiments. The jars were put on a roller (7–8 r/min) at room temperature (25 ± 1 °C) for four weeks until the partitioning equilibrium of PAHs between sediment and PDMS was achieved (Li et al., 2016). The exposed PDMS was collected and then sonicated with 15 mL of mixture of hexane and acetone (1:1, V/V) twice for 10 min each. Finally, the

PDMS extracts were reduced to approximately 1 mL under a gentle stream of nitrogen and stored at −20 °C until further analysis. Upon equilibration, freely dissolved concentration of PAHs in sediment pore water (Cfree-sed, ng/L) can be calculated according to Eq. (1) (Li et al., 2013). C free−sed ¼

C PDMS K PDMSw

ð1Þ

where CPDMS is the concentration of PAHs that partitioned into PDMS, ng/gPDMS; KPDMSw is the partition coefficient of PAHs between PDMS and water, Lw/gPDMS. The KPDMSw values for the 16 targeted PAHs were derived from previous studies, and mean values were used for subsequent calculations (Table S2). 2.4. Stable isotope analysis The pretreatment procedure for trophic level analysis was described in the previous report (Qu et al., 2016). Briefly, each tissue sample was cut into small pieces, placed in an oven at 80 °C for at least 48 h until constant weight was achieved, and then ground into fine powder using mortar and pestle. The isotopic composition of nitrogen in samples was analyzed using vario EL III element analyzer coupled with isotope ratio mass spectrometer (Germany Elementar company). 2.5. Chemical analysis The 16 USEPA PAH congeners in seawater, sediment, marine organisms and PDMS were quantified by gas chromatography–mass spectrometry (GC–MS, Agilent 7890A/5975C) following our previously reported method (Li et al., 2015b). Briefly, DB-5MS column (30 m × 0.25 mm × 0.25 μm) was applied, using helium as carrier gas with a flowrate of 0.2 mL/min. The injection temperature was 280 °C using the splitless injection mode with an injection volume of 2 μL. The initial oven temperature of 100 °C increased to 190 °C at 15 °C/min, to 215 °C at 6 °C/min, to 280 °C at 20 °C/min, held for 10 min, and finally to 310 °C at 20 °C/min, held for 2 min. The PAH standards (N99%) were purchased from Sigma Aldrich. 2.6. QA/QC All samples were spiked with PAH surrogate standards prior to extraction, naphthalene-d8, acenaphthylene-d10, phenanthrene-d10, chrysene-d12 and perylene-d12 were used to correct the amounts of specific PAHs (1) NAP; (2) ANY, ANA, and FLU; (3) PHE, ANT, FLT and

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PYR; (4) CHR and BaA; and (5) BbF, BkF, BaP, DBA, IPY, and BghiP, respectively, detected in the samples. Recoveries of the above PAH surrogate standards were 50.9 ± 13.6%, 58.4 ± 10.8%, 78.4 ± 5.6%, 81.9 ± 7.1% and 92.4 ± 9.7% respectively. Detection limits and recoveries of the analytes in different environmental media were listed in Table S3.

Trophic magnification factors (TMFs) were computed based on the regression of PAH concentration versus TL according to the following equations:

2.7. Data analysis

TMF ¼ 10a

2.7.1. Derivation of thermodynamic potentials of PAHs for bioaccumulation The thermodynamic potential of PAHs in benthic organisms for bioaccumulation is indicated by the lipid-based concentrations at equilibrium condition (Cbenthic-lip, ng/glip), which can be calculated as follows (Jahnke et al., 2014b), C benthic−lip ¼ C PDMS  K lip−PDMS

ð2Þ

where CPDMS (ng/gPDMS) is the concentration of PAHs in PDMS and Klip-PDMS (gPDMS /glip) is the partition coefficient between lipid and PDMS. In the present study, Klip-PDMS value of 30 was applied according to our previous research (Li et al., 2016; Jin et al., 2013). Instead of concentration in sediments, Cbenthic-lip is a more reliable parameter to evaluate the potential risk of HOCs in sediment (Jahnke et al., 2014a; Li et al., 2018; Jahnke et al., 2014b). All values of CPDMS and CPDMS-lip were shown in Table S4. For the pelagic organisms living in the upper layer of the seawater, the freely dissolved concentration of PAHs in overlying water (Cfreewater, ng/L) is the driving force for the bioaccumulation (Yang et al., 2006; Kukkonen et al., 1989). The lipid-based tissue concentrations of PAHs at equilibrium in pelagic species (Cpelagic-lip, ng/glip) can be calculated according to the following equations. C pelagic−lip ¼ C free−water  K lipw C free−water ¼

C field−water 1 þ K DOC  DOC

ð3Þ ð4Þ

where Cfield-water (ng/L) is the PAH concentrations in surface seawater measured using GC–MS (Table S4). The literature values of KDOC (L/ kgDOC) and Klipw (Lw/glip) were provided in Table S2. The measured DOC was 7.2 ± 0.9 mg/L.

log½PAH concentration ¼ a  TL þ b

ð7Þ ð8Þ

2.7.3. Risk assessment In the present study, the dietary carcinogenic risks posed by PAHs were evaluated according to the incremental lifespan cancer risk (ILCR) based on the guidance proposed by EPA (USEPA, 1993). The equations were given as follows. ILCR ¼

BaP eq  CSF ingestion  IR  EF  ED BW  AT

ð9Þ

where, EF, ED, BW and AT are exposure frequency (EF, 365 day year−1in this study), exposure duration (ED, 30 years for ILCR estimation), body weight (BW, 55 kg in this study) and average time (AT, 25,550 days in the present study), respectively. BaPeq is the BaP toxic equivalent concentration of carcinogenic PAHs (USEPA, 1993), which includes CHR, BaA, BbF, BkF, BaP, DBA, IPY, and BghiP. The oral cancer slope factor (CSF) was set at7.3 (mg kg−1 day−1)−1 in Eq. (7). The daily ingestion rates (IR, g day−1) of different organisms were sought from literatures and set to be 110.5 and 93.43 g day−1 (wet weight) for fish (C. lucidus, C. mystus, H. nehereus, C. nasus, S. elongate, C. myriaster, C. robutus, P. anomala, J. belangerii, and L. litulon), mollusks (S. cucullata, N. schrenckii, M. veneriformis, N. yoldi, D. japonica, B. canaliculatu, and S. constricta) and crustaceans (T. curvirostris and L. crocea) species, respectively (Table S5). All figures in the present study were plotted using GraphPad Prism6 (GraphPad Software, Inc., USA) with the data presented as mean ± standard deviation (SD). Pearson's rank correlation test was used to examine the relationship between trophic level and logarithmic concentration of PAHs. One-way ANOVA was performed to compare the difference between groups using SPSS 19.0 for windows (SPSS Inc., USA). Statistical significance was considered at p b 0.05. 3. Results and discussion

2.7.2. Trophic level calculation Stable isotope ratios of nitrogen (δ) were determined as follows: 15

δ15 Nð‰Þ ¼

N=14 Nsample

15 N=14 N

−1Þ  1000

ð5Þ

air

where 15N/14Nsample is the ratio of the heavy isotope to the light isotope in tissue sample and 15N/14Nair represents the ratio of the heavy isotope to the light isotope in the atmosphere. Triplicate determinations were performed for each sample with the standard deviation of ±0.2‰ for δ15N. Nitrogen isotope can be magnified through the food chain, and the trophic levels of different marine organisms can be estimated according to Eq. (6): TL ¼

δ15 Npred −δ15 Nbase δ15 NTEF

þ TLbase

ð6Þ

where TL is the trophic level, δ15Npred is the nitrogen isotope ratio of the predator, δ15Nbase is the nitrogen isotope ratio of the baseline animal (S. cucullata in the present study), and δ15NTEF is the enrichment factors. In this study, the δ15NTEF value of 3.4‰ was applied according to the previous study (Post et al., 2000). TLbase is the trophic level of the baseline animal and is assumed to be 2.

3.1. Altered bioavailability and sediment-water flux of PAHs ΣPAHs in surface seawater in the operation phrase ranged from 29 to 77 ng/L (Fig. 2 and Table S6), which underwent 1 order of magnitude decline, compared with those in the construction phase (110–860 ng/L). A two-fold decrease was also seen with ΣPAHs in sediment from the construction phase (120–780 ng/g dw) to the operation phase (104–233 ng/g dw) (Fig. 2 and Table S6). Before 2015, a number of hydraulic projects, such as submarine pipeline installation, bridge pier construction, land reclamation, and oil depot construction, took place in the construction phase. These extensive infrastructure and transportation activities led to crude oil-related contamination, particularly by high levels of ∑PAHs in port waters with dominance of low molecular weight PAH congeners (Li et al., 2015b). In transition to the operation phase, the port underwent large-scale ecological remediation measures, which contributed to the decrease in the bulk burden of PAHs in the surface water. We further measured the Cfree of PAHs in surface seawater and sediment using PDMS polymer-based passive sampling in the construction and operation phases. In consistency with the reduced bulk concentrations of ΣPAHs, Cfree of PAHs in surface sea water in the operation phase (15–53 ng/L) declined by one order of magnitude compared with those in the construction phase (105–821 ng/L), while Cfree of PAHs in sediment pore water did not show a significant decline (Fig. 2 and

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Fig. 2. Concentrations of ∑PAHs (left panel: bulk concentrations; right panel: freely-dissolved bioavailable concentrations) in surface seawater and sediment in the waters of Yangshan Port transitioning from construction to operation. The bottom and top of the box refer to the 25th and 75th percentiles (lower and upper quartiles) of the total concentration or Cfree of PAHs in sediments or overlying seawaters. The line in the middle of the box is the 50th percentile (the median). The end whiskers represent the min and max of all the data on bulk concentrations or Cfree of PAHs.

Table S6). As freely dissolved aqueous concentration is a measure of chemical activity, the difference in Cfree in sediment porewater and overlaying seawater sensed by the passive sampler indicates the direction of the chemical flux. For instance, the ratio of Cfree in sediment porewater (Cfree-sed) to that in overlaying seawater (Cfree-water) N 1 suggests an upward flux of PAHs from sediment to overlaying water (Beckingham and Ghosh, 2013) and vice versa. In the construction phase, the Cfree-water/Cfree-sed ratios were all higher than or close to 1 for each PAH congener (Fig. 3), demonstrating the higher chemical activity and higher bioavailability of PAHs in overlaying seawater and hence a downward flux of PAHs from overlaying water to sediment. By contrast, the Cfree-water/Cfree-sed ratios in the operation phase were mostly lower than or close to 1 (Fig. 3), implying higher chemical activity of PAHs in sediment and an opposite PAH flux direction. These changes in bulk and bioavailable concentrations and sediment-water fluxes of PAHs suggested the positive impacts of joint measures including point source controls and ecological remediation in the port waters after the construction phase. 3.2. Reduced tissue residues and risks of PAHs in marine organisms Fig. 4 shows that concentrations of ΣPAHs in the oysters (S. cucullata) detected in the operation phase (990 ng/g dw; Table S7) dropped by 1 order of magnitude compared to those detected earlier

in the construction phase (1100–29,000 ng/g dw; Li et al., 2015b). The incremental lifetime cancer risks (ILCR) via consuming oysters from Yangshan Port over a 70-years exposure to 16 US-EPA PAHs (Ding et al., 2012) also dropped 2–3 orders of magnitude (Fig. 4). The decline of ΣPAHs in the oyster corresponded to the altered flux and bioavailability of PAHs at the sediment-water interface. In the construction phase, the surface seawater instead of the sediment porewater drove the accumulation of PAHs in the oyster, owing to the downward PAH fluxes from the overlying seawater to sediment (Li et al., 2015b; Fig. 3). Contrastively, in the operation phase, the sediment porewater became the quantitative driving force of PAH accumulation in the oyster (Fig. 5). Altered flux and bioavailability of PAHs at the sediment-water interface in different phases of the port was directly related to a series of remediation measures taken during the period, and highlighted the effectiveness of the remediation efforts in the port area. In addition to the oyster (S. cucullata), we also evaluated the tissue residues and associated risks of PAHs in 8 benthic and 11 pelagic species, which were collected in the operation phase only. ΣPAHs varied dramatically among all species of marine organisms, ranging from 1074 to 22,917 ng/glip (Table S7), which are comparable to the levels in the marine organisms from other port/harbor areas (Fig. S1). The concentrations of ΣPAHs in the benthic species (9220 to 22,917 ng/glip) were remarkably higher than those in the pelagic species (1074–14,913 ng/glip) (Fig. 5; Table S7). Although the 3- and 4-ring PAHs

Fig. 3. Comparison of congener-specific chemical activity of PAHs between sediment porewater and overlying seawater indicated by the ratio of Cfree-sed to Cfree-water (the error bar represents the standard deviation).

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were still the predominant congeners in most of the species, contributing 59–100% of ΣPAHs (Table S7 and Fig. S2), the percentage of 3-ring PAHs increased obviously and the predominant congeners (FLT, PYR, CHR and BaA in the present study) also showed a tendency to move to the individuals of low molecular weight compared with the result (BaA, BbF and BkF) reported previously (Li et al., 2015b). Potentially carcinogenic PAHs (including BaA, BbF, BkF, BaP, DBA, and BghiP) in marine organisms ranged from 5.9 to 340 ng/g dw (Table S7) and contributed 1.2–29% of ΣPAHs, suggesting a remarkable decrease both in concentration and in percentage. ILCR ranged from 1.94 × 10−8 to 1.47 × 10−5 (Table S7) and most species were lower than the acceptable guideline value of 1 × 10−6 except several organisms with higher trophic level including T. curvirostris, C. myriaster, P. anomala, and L. litulon. 3.3. Predictive utility of equilibrium sampling in linking bioavailability and bioaccumulation and in evaluating remediation effectiveness The bioaccumulation factors of PAHs in marine organisms from Yangshan Port (Fig. S3) were higher than those bioaccumulative compounds with BAF values N5000 L/kg in fish on a wet weight basis (Arnot and Gobas, 2006; Conder et al., 2008). The comparison suggested great bioaccumulation potential of PAHs in marine organisms dwelling in the port area, although concentrations of individual congeners and total PAHs underwent a considerable decline. Generally, concentrations of PAHs in benthic species with lower trophic levels were remarkably higher than those in pelagic species with higher trophic levels, resulting in the apparent “trophic dilution” of PAHs in the whole marine food web (Fig. 5). This observation was consistent with the previous studies in Arika Sea (Nakata et al., 2003), Tokoyo Bay (Takeuchi et al., 2009), Bohai (Wan et al., 2007), Dianchi (Fan et al., 2017), and Baltic Sea (Nfon et al., 2008). The higher body burdens of PAHs in benthic organisms compared with those in pelagic organisms may be attributed to the higher values of both Cfree in sediment porewater and bulk burdens in the sediments (Table S4). Furthermore, sediments are important food sources for some benthic organisms, and the dietary uptake from the sediments might dominate the body burden of PAHs in benthic organisms (Wang et al., 2019). In addition, cytochromes P450, which catalyze the oxidation of various chemicals, are relatively poor in benthic species at lower trophic levels, resulting in lower metabolic capability for biotransformation (Wan et al., 2007). We compared the tissue residues of PAHs in marine organisms measured instrumentally with the thermodynamic potentials of PAHs for bioaccumulation in benthic and pelagic species based on equilibrium partitioning-based calculation using Eqs. (2) and (3). In consistency

with the measured concentrations of ΣPAHs in benthic and pelagic species (scattered points in Fig. 5), the predicted range of thermodynamic potential of PAHs for bioaccumulation (shaded area in Fig. 5) in the benthic species was also generally higher than that in the pelagic species. The shadows clearly evidenced that the thermodynamic potentials for bioaccumulation of PAHs differed between benthic and pelagic habitats with no overlap. Most species dwelling in either habitat had concentrations of PAHs falling within the range of thermodynamic potentials for bioaccumulation in the corresponding habitat. While PAH concentrations were generally constant among the benthic species across trophic levels (Fig. 5), trophic magnification of PAHs was observed in the pelagic species with a TMF of ~10, as shown by the linear regression between the logarithmic lipid-based concentration of ΣPAHs and the trophic levels (Figs. 5 and S4). FLT, PYR and BaA, three congeners dominating the PAH composition profiles, were also the major drivers underlying the trophic transfer of PAHs in the pelagic community. Each of them had a TMF of ~10 (Fig. S4). The differences in trophic transfer between the pelagic and benthic species can be partially explained by higher lipid levels of the pelagic biota (mean: 9.54%, Table S1) when compared to those of the benthic biota (mean: 5.34%, Table S1). Gobas et al. (1999) and Kidd et al. (2001) observed that predators may incorporate larger amounts of organochlorines and DDT from lipid-rich prey when compared to lipid-poor prey species, respectively. Furthermore, different dietary uptake patterns in benthic and pelagic species also lead to different ingestion amounts of HOCs, thus influencing the body burden and trophic magnification of HOCs in organisms (Wang et al., 2019). Therefore, the oyster and a pelagic species at the higher trophic level (e.g., C. nasus abundant in the Zhoushan fishing ground, adjacent to Yangshan Port) can be model species for future long-term monitoring of environmental changes in the port waters. The differing bioaccumulation of PAHs between the benthic and pelagic communities may be determined by different living habitats where the bioavailability of PAHs varies (Wang et al., 2016). Specifically, benthic species dwell in sediment or attach themselves to rocks near sediment, and therefore the equilibrium of PAHs between sediment pore water and the benthic species was relatively easily achieved. For pelagic species living in the upper layer of the seawater, Cfree-water instead of Cfree-sed was the main driving force for the bioaccumulation of PAHs (Yang et al., 2006; Kukkonen et al., 1989) and Cfree-water provided a better estimate for the tissue concentrations of PAHs in pelagic species, supporting the habitat-specific bioavailability and exposure pathways of PAHs. Earlier studies also confirmed that clear deviations between measured and predicted concentrations in aquatic organisms were evident when chemical activity of organic contaminants was clearly higher in sediment than that in overlying water in a freshwater lake (Mäenpää et al., 2011; Mäenpää et al., 2015). Moreover, the PAHs fluxes also suggested that the body residue of PAHs in the benthic would remain relatively stable if no additional significant input of PAHs was introduced. On the contrary, for the pelagic environment, the upward flux from sediment porewater would compensate the concentration and chemical activity of PAHs in the overlying water, and lead to the further increase in PAH residues in pelagic species in the future. Therefore, Cfree sensed by passive sampling not only estimates the bioavailability of PAHs, but also predicts their bioaccumulation potential quantitatively, which is of high practical value in evaluating remediation effectiveness to alleviate ecological risks. 4. Conclusions

Fig. 4. Comparison of bulk PAH concentrations and incremental lifetime cancer risks (ILCRs) in oysters between the construction and the operation phases.

Owing to the efforts dedicated to ecological restoration, contamination and ecological risks of PAHs were remarkably reduced in the multimedia environment of Yangshan Port. The reduced bioavailability and altered fluxes at the sediment-water interface measured by PDMS-based equilibrium sampling was mechanistically linked to the reduced bioaccumulation and risks in marine organisms. Our study also demonstrated that thermodynamics-based equilibrium sampling and

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Fig. 5. Measured concentrations of ΣPAHs (in circle) in benthic and pelagic species (Cbio,lip, ng/glip) and comparison with thermodynamic potentials of PAHs calculated based on Cfree. Scattered points represent the measured concentrations of ΣPAHs in marine animals. The shaded area represents the min-max range of thermodynamic potentials of PAHs for bioaccumulation in benthic and pelagic species, which were calculated according to Eqs. (2) and (3), respectively.

partitioning theory can be a robust tool to quantify the driving forces underlying the remediation effectiveness. Therefore, equilibrium partitioning-based approaches, such as passive sampling, offer powerful tools for risk assessment in multi-trophic environment, and may benefit the remediation measures for contaminated marine sites. Acknowledgements This research is funded by the Science and Technology Commission of Shanghai Municipality (18050502100) and Shanghai Collaborative Innovation Center for Aquatic Animal Genetics and Breeding (A12037-17-000112), respectively. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2019.06.040. References Arnot, J.A., Gobas, F.A.P.C., 2006. A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environ. Rev. 14, 257–297. Beckingham, B., Ghosh, U., 2013. Polyoxymethylene passive samplers to monitor changes in bioavailability and flux of PCBs after activated carbon amendment to sediment in the field. Chemosphere 91, 1401–1407. Burns, K.A., 2014. PAHs in the Great Barrier Reef Lagoon reach potentially toxic levels from coal port activities. Estuar. Coast. Shelf Sci. 144, 39–45. Casado-Martinez, M.C., Branco, V., Vale, C., Ferreira, A.M., DelValls, T.A., 2008. Is Arenicola marina a suitable test organism to evaluate the bioaccumulation potential of Hg, PAHs and PCBs from dredged sediments. Chemosphere 70, 1756–1765. Conder, J.M., Hoke, R.A., Wolf, W.D., Russell, M.H., Buck, R.C., 2008. Are PFCAs bioaccumulative? A critical review and comparison with regulatory criteria and persistent lipophilic compounds. Environ. Sci. Technol. 42, 995–1003. Ding, C., Ni, H.G., Zeng, H., 2012. Parent and halogenated polycyclic aromatic hydrocarbons in rice and implications for human health in China. Environ. Pollut. 168, 80–86. Fan, S., Wang, B., Liu, H., Gao, S., Li, T., Wang, S., Liu, Y., Liu, X., Wan, Y., 2017. Trophodynamics of organic pollutants in pelagic and benthic food webs of Lake Dianchi: importance of ingested sediment as uptake route. Environ. Sci. Technol. 51, 14135–14143. Figueiredo, K., Mäenpää, K., Lyytikäinen, M., Taskinen, J., Leppänen, M.T., 2017. Assessing the influence of confounding biological factors when estimating bioaccumulation of PCBs with passive samplers in aquatic ecosystems. Sci. Total Environ. 601–602, 340–345. Gobas, F.A.P.C., Wilcockson, J.B., Russell, R.W., Haffner, G.D., 1999. Mechanism of biomagnification in fish under laboratory and field conditions. Environ. Sci. Technol. 33, 133–141. Hunter, W., Xu, Y., Spurlock, F., Gan, J., 2008. Using disposable polydimethylsiloxane fibers to assess the bioavailability of permethrin in sediment. Environ. Toxicol. Chem. 27, 568–575. Jager, T., Baerselman, R., Dijkman, E., Groot, A.C.D., Hogendoorn, E.A., Jong, A.D., Kruitbosch, J.A.W., Peijnenburg, W.J.G.M., 2003. Availability of polycyclic aromatic hydrocarbons to earthworms (Eisenia andrei, oligochaeta) in field-polluted soils and soil-sediment mixtures. Environ. Toxicol. Chem. 22, 767–775.

Jahnke, A., MacLeod, M., Wickstrom, H., Mayer, P., 2014a. Equilibrium sampling to determine the thermodynamic potential for bioaccumulation of persistent organic pollutants from sediment. Environ. Sci. Technol. 48, 11352–11359. Jahnke, A., Mayer, P., McLachlan, M.S., Wickstrom, H., Gilbert, D., MacLeod, M., 2014b. Silicone passive equilibrium samplers as 'chemometers' in eels and sediments of a Swedish lake. Environ. Sci. Process. Impacts 16, 464–472. Jin, L., Gaus, C., Van, M.L., Escher, B.I., 2013. Applicability of passive sampling to bioanalytical screening of bioaccumulative chemicals in marine wildlife. Environ. Sci. Technol. 47, 7982–7988. Kidd, K.A., Bootsma, H.A., Hesslein, R.H., Muir, D.C., Hecky, R.E., 2001. Biomagnification of DDT through the benthic and pelagic food webs of Lake Malawi, East Africa: importance of trophic level and carbon source. Environ. Sci. Technol. 35, 14–20. Kim, C.J., Hong, G.H., Kim, H.E., Yang, D.B., 2014. Polycyclic aromatic hydrocarbons (PAHs) in starfish body and bottom sediments in Mohang Harbor (Taean), South Korea. Environ. Monit. Assess. 186, 4343–4356. Kong, X., He, W., Qin, N., Liu, W., Yang, B., Yang, C., Xu, F., Mooij, W.M., Koelmans, A.A., 2017. Integrated ecological and chemical food web accumulation modeling explains PAHs temporal trends during regime shifts in a shallow lake. Water Res. 119, 73–82. Kukkonen, J., Oikari, A., Johnsen, S., Gjessing, E., 1989. Effects of humus concentrations on benzo a pyrene accumulation from water to Daphnia magna: comparison of natural waters and standard preparations. Sci. Total Environ. 79, 197–207. Lacroix, C., Richard, G., Seguineau, C., Guyomarch, J., Moraga, D., Auffret, M., 2015. Active and passive biomonitoring suggest metabolic adaptation in blue mussels (Mytilus spp.) chronically exposed to a moderate contamination in Brest harbor (France). Aquat. Toxicol. 162, 126–137. Lang, S.C., Hursthouse, A., Mayer, P., Kotke, D., Hand, I., Schulz-Bull, D., Witt, G., 2015. Equilibrium passive sampling as a tool to study polycyclic aromatic hydrocarbons in Baltic Sea sediment pore-water systems. Mar. Pollut. Bull. 101, 296–303. Li, J.Y., Tang, J.Y.M., Jin, L., Escher, B.I., 2013. Understanding bioavailability and toxicity of sediment-associated contaminants by combining passive sampling with in vitro bioassays in an urban river catchment. Environ. Toxicol. Chem. 32, 2888–2896. Li, J., Li, Z., Cui, Y., Hu, Q., Chen, M., Zheng, Y., 2015a. Biomimetic research on bioavailability and bioaccumulation of sediment-associated pyrethroids using solid-phase microextraction. Asian Journal of Ecotoxicology 10, 144–152. Li, J.Y., Cui, Y., Su, L., Chen, Y., Jin, L., 2015b. Polycyclic aromatic hydrocarbons in the largest deepwater port of East China Sea: impact of port construction and operation. Environ. Sci. Pollut. Res. 22, 12355–12365. Li, J., Dong, H., Zhang, D., Han, B., Zhu, C., Liu, S., Liu, X., Ma, Q., Li, X., 2015c. Sources and ecological risk assessment of PAHs in surface sediments from Bohai Sea and northern part of the Yellow Sea, China. Mar. Pollut. Bull. 96, 485–490. Li, J.Y., Su, L., Wei, F., Yang, J., Jin, L., Zhang, X., 2016. Bioavailability-based assessment of aryl hydrocarbon receptor-mediated activity in Lake Tai Basin from Eastern China. Sci. Total Environ. 544, 987–994. Li, J.Y., Shi, W., Li, Z., Chen, Y., Shao, L., Jin, L., 2018. Equilibrium sampling informs tissue residue and sediment remediation for pyrethroid insecticides in mariculture: a laboratory demonstration. Sci. Total Environ. 616-617, 639–646. Mäenpää, K., Matti, T., Leppänen, F.R., Kaisa, F., Mayer, P., 2011. Equilibrium sampling of persistent and bioaccumulative compounds in soil and sediment: comparison of two approaches to determine equilibrium partitioning concentrations in lipids. Environ. Sci. Technol. 45, 1041–1047. Mäenpää, K., Matti, T., Leppänen, Kaisa, F., Feven, T.S., Reijo, K., 2015. Sorptive capacity of membrane lipids, storage lipids, and proteins: a preliminary study of partitioning of organochlorines in lean fish from a PCB-contaminated freshwater lake. Arch. Environ. Contam. Toxicol. 68, 193–203. Mayer, P., Vaes, W.H., Hermens, J.L., 2000. Absorption of hydrophobic compounds into the poly (dimethylsiloxane) coating of solid-phase microextraction fibers: high partition coefficients and fluorescence microscopy images. Anal. Chem. 72, 459–464. Mayer, P., Parkerton, T.F., Adams, R.G., Cargill, J.G., Gan, J., Gouin, T., Gschwend, P.M., Hawthorne, S.B., Helm, P., Witt, G., You, J., Escher, B.I., 2014. Passive sampling

686

J.-Y. Li et al. / Science of the Total Environment 687 (2019) 679–686

methods for contaminated sediments: scientific rationale supporting use of freely dissolved concentrations. Integr. Environ. Assess. Manag. 10, 197–209. Nakata, H., Sakai, Y., Miyawaki, T., Takemura, A., 2003. Bioaccumulation and toxic potencies of polychlorinated biphenyls and polycyclic aromatic hydrocarbons in tidal flat and coastal ecosystems of the Ariake Sea, Japan. Environ. Sci. Technol. 37, 3513–3521. Nasher, E., Heng, L.Y., Zakaria, Z., Surif, S., 2016. Health risk assessment of polycyclic aromatic hydrocarbons through aquaculture fish consumption, Malaysia. Environ. Forensic 17, 97–106. Nfon, E., Cousins, I.T., Broman, D., 2008. Biomagnification of organic pollutants in benthic and pelagic marine food chains from the Baltic Sea. Sci. Total Environ. 397, 190–204. Parinos, C., Gogou, A., 2016. Suspended particle-associated PAHs in the open eastern Mediterranean Sea: occurrence, sources and processes affecting their distribution patterns. Mar. Chem. 180, 42–50. Pérez-Fernández, B., Viñas, L., Franco, M.Á., Bargiela, J., 2015. PAHs in the Ría de Arousa (NW Spain): a consideration of PAHs sources and abundance. Mar. Pollut. Bull. 95, 155–165. Post, D.M., Pace, M.L., Hairston, N.G., 2000. Ecosystem size determines food-chain length in lakes. Nature 405, 1047–1049. Qu, P., Wang, Q., Pang, M., Zhang, Z., Liu, C., Tang, X., 2016. Trophic structure of common marine species in the Bohai Strait, North China Sea, based on carbon and nitrogen stable isotope ratios. Ecol. Indic. 66, 405–415. Ramdine, G., Fichet, D., Louis, M., Lemoine, S., 2012. Polycyclic aromatic hydrocarbons (PAHs) in surface sediment and oysters (Crassostrea rhizophorae) from mangrove of Guadeloupe: levels, bioavailability, and effects. Ecotoxicol. Environ. Saf. 79, 80–89. Ruiz-Fernández, A.C., Betancourt, P.J.M., Sericano, J.L., Sanchez, C.J.A., Espinosa, L.F., Cardoso, M.J.G., Pérez, B.L.H., Garay, T.J.A., 2016. Coexisting sea-based and landbased sources of contamination by PAHs in the continental shelf sediments of Coatzacoalcos River discharge area (Gulf of Mexico). Chemosphere 144, 591–598. Samuelsson, G.S., Hedman, J.E., Krusa, M.E., Gunnarsson, J.S., Cornelissen, G., 2015. Capping in situ with activated carbon in Trondheim harbor (Norway) reduces bioaccumulation of PCBs and PAHs in marine sediment fauna. Mar. Environ. Res. 109, 103–112. Simpson, C.D., Mosi, A.A., Cullen, W.R., Reimer, K.J., 1996. Composition and distribution of polycyclic aromatic hydrocarbon contamination in surficial marine sediments from Kitimat Harbor, Canada. Sci. Total Environ. 181, 265–278.

Takeuchi, I., Miyoshi, N., Mizukawa, K., Takada, H., Ikemoto, T., Omori, K., Tsuchiya, K., 2009. Biomagnification profiles of polycyclic aromatic hydrocarbons, alkylphenols and polychlorinated biphenyls in Tokyo Bay elucidated by δ13C and δ15N isotope ratios as guides to trophic web structure. Mar. Pollut. Bull. 58, 663–671. Thomas, C., Lampert, D., Reible, D., 2014. Remedy performance monitoring at contaminated sediment sites using profiling solid phase microextraction (SPME) polydimethylsiloxane (PDMS) fibers. Environ. Sci. Process. Impacts 16, 445–452. Tuikka, A.I., Leppänen, M.T., Akkanen, J., Sormunen, A.J., 2016. Predicting the bioaccumulation of polyaromatic hydrocarbons and polychlorinated biphenyls in benthic animals in sediments. Sci. Total Environ. 563–564, 396–404. USEPA, 1993. Provisional Guidance for Quantitative Risk Assessment of Polycyclic Aromatic Hydrocarbons. Development. United States Environmental Protection Agency. Varnosfaderany, M.N., Bakhtiari, A.R., Gu, Z., Chu, G., 2014. Vertical distribution and source identification of polycyclic aromatic hydrocarbons (PAHs) in southwest of the Caspian Sea: Most petrogenic events during the late Little Ice Age. Mar. Pollut. Bull. 87, 152–163. Wan, Y., Jin, X., Hu, J., Jin, F., 2007. Trophic dilution of polycyclic aromatic hydrocarbons (PAHs) in a marine food web from Bohai Bay, north China. Environ. Sci. Technol. 41, 3109–3114. Wang, Z.H., Chen, Y., Zhang, S.Y., Wang, K., Zhao, J., Xu, Q., 2015. A comparative study of fish assemblages near aquaculture, artificial and natural habitats. J. Ocean U. China 14, 149–160. Wang, J., Bi, Y., Henkelmann, B., Pfister, G., Zhang, L., Schramm, K.W., 2016. PAHs and PCBs accumulated by SPMD-based virtual organisms and feral fish in Three Gorges Reservoir, China. Sci. Total Environ. 542, 899–907. Wang, H.T., Xia, X.H., Liu, R., Wang, Z.X., Zhai, Y.W., Lin, H., Wen, W., Li, Y., Wang, D.H., Yang, Z.F., Derek, Muir, G, C., Crittenden, J.C., 2019. Dietary uptake patterns affect bioaccumulation and biomagnification of hydrophobic organic compounds in fish. Environ. Sci. Technol. 53, 4274–4284. Xue, R., Chen, L., Lu, Z., Wang, J., Yang, H., Zhang, J., Cai, M., 2016. Spatial distribution and source apportionment of PAHs in marine surface sediments of Prydz Bay, East Antarctica. Environ. Pollut. 219, 528–536. Yang, W.C., Spurlock, F., Liu, W.P., Gan, J.Y., 2006. Effects of dissolved organic matter on permethrin bioavailability to Daphnia species. J. Agric. Food Chem. 54, 3967–3972.