Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea

Marine Pollution Bulletin xxx (2014) xxx–xxx

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea Chin-Chang Hung a,b,⇑, Fung-Chi Ko c,d, Gwo-Ching Gong b,e, Kuo-Shu Chen a, Jian-Ming Wu e, Hsin-Lun Chiang e, Sen-Chueh Peng f, Peter H. Santschi g a

Department of Oceanography and Asia-Pacific Ocean Research Center, National Sun Yat-sen University, Kaohsiung 80424, Taiwan Taiwan Ocean Research Institute, National Applied Research Laboratories, Kaohsiung, Taiwan National Museum of Marine Biology and Aquarium, Pingtung 94450, Taiwan d Institute of Marine Biodiversity and Evolutionary Biology, National Dong Hwa University, Pingtung 94450, Taiwan e Institute of Marine Environmental Chemistry and Ecology, National Taiwan Ocean University, Keelung 20224, Taiwan f Department of Electrical Engineering, National Formosa University, Yunlin 63201, Taiwan g Department of Marine Sciences, Laboratory for Oceanography and Environmental Research, Texas A&M University at Galveston, 200 Seawolf Parkway, Galveston, TX 77553, USA b c

a r t i c l e Keywords: PAH Zooplankton East China Sea Salinity front

i n f o

a b s t r a c t The Changjiang has transported large quantities of polycyclic aromatic hydrocarbons (PAHs) to the East China Sea (ECS), but information of these pollutants in zooplankton is limited. To understand PAHs pollution in zooplankton in the ECS, total concentrations of PAHs in zooplankton from surface waters were measured. Values of PAHs ranged from 2 to 3500 ng m 3 in the ECS, with highest PAHs levels located at the salinity front between the Changjiang Diluted Water (CDW) and the mid-shelf waters. In contrast, concentrations of zooplankton PAHs in the mid-shelf and outer-shelf waters were significantly lower (2–23 ng m 3) than those in the CDW. These results demonstrate that PAHs are conspicuously accumulated in zooplankton at the salinity front between the CDW and the mid-shelf waters. These higher levels of PAHs in zooplankton at the salinity front may be further biomagnified in marine organisms of higher trophic levels through their feeding activities. Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

1. Introduction Frontal zones are important features in the ocean (Olson et al., 1994; Nakata et al., 2000; Kasai et al., 2002; Longhurst, 2006). Oceanic frontal systems are frequently observed in estuaries, coastal regions and marginal seas due to several different physical mechanisms generating fronts, such as density gradients from terrestrial water discharge, tidal mixing, coastal wind-forced upwelling, and wintertime thermal convection (Belkin et al., 2009). These physical processes also greatly affect the chemical composition of oceanic frontal systems. For example, as a result of river freshwater discharge, river plume fronts are characterized by enriched terrestrial substances (Atkinson et al., 1983; Belkin et al., 2009). Owing to terrestrial nutrient supply, river plume fronts are particularly important for phytoplankton growth in coastal ecosystems and are beneficial to the enhancement of local ⇑ Corresponding author at: Department of Oceanography and Asia-Pacific Ocean Research Center, National Sun Yat-sen University, 70 Lien-Hai Rd, Kaohsiung 80424, Taiwan. Tel./fax: +886 7 525 5490. E-mail address: [email protected] (C.-C. Hung).

fisheries resources (Kingsford and Suthers, 1994; John et al., 2001). Moreover, it has long been thought that oceanic fronts can concentrate pollutants, such as heavy metals (Kremling, 1983; Balls, 1985) and polychlorinated biphenyls (PCBs); however, field observations of polycyclic aromatic hydrocarbons (PAHs) have rarely been conducted in oceanic frontal zones. PAHs are often produced by incomplete fossil fuel burning and accidental discharges of petroleum products from factories, vehicles, and ships (Fang et al., 2003; Doong and Lin, 2004; Ko and Baker, 2004; Froehner et al., 2010). They have been declared as primary pollutants by the Environmental Protection Agency, United States, due to their carcinogenicity, toxicity, and mutagenicity. Recent research has shown that PAHs can be transported from terrestrial sources to estuaries and nearby coastal areas via discharges and land runoff (Gogou et al., 1996; Bouloubassi et al., 2001; Li et al., 2006; Hung et al., 2010, 2011; Cheng et al., 2010; Ko et al., 2014a). After PAHs have been transported to estuarine and coastal environments through various physical processes, they will be incorporated with phytoplankton or detritus. Subsequently, they may enter marine food chains to be highly accumulated in marine organisms of higher trophic levels (e.g., zooplankton, fish

http://dx.doi.org/10.1016/j.marpolbul.2014.03.045 0025-326X/Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

Please cite this article in press as: Hung, C.-C., et al. Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.045

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C.-C. Hung et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

larvae, fishes, or mammals) via absorption and/or bioaccumulation (Landrum et al., 1992; Burkhard, 1998; Cailleaud et al., 2007; Vigano et al., 2007; Froehner et al., 2010; Hung et al., 2011; Ko et al., 2014b). Therefore, an understanding of how PAHs are distributed and accumulated in zooplankton contributes to a better understanding of PAHs pollution in marine ecosystems. The East China Sea (ECS) is a large marginal sea of the Pacific Ocean and is characterized by high values of primary production, particulate organic carbon flux, carbohydrate yield, and carbon sequestration rate (Gong et al., 2003, 2006, 2011; Hung et al., 2009a, 2010, 2013; Chen et al., 2013a; Chou et al., 2009, 2011, 2013). The ECS also supports many key fisheries stocks, e.g., croakers, mackerels, hairtails, and pomfrets (Chen et al., 1997; Hung and Gong, 2011). According to previous studies, distinct salinity fronts have been frequently found in the ECS and may be important for small fish and plankton (Belkin et al., 2009; Chen, 2009). Besides numerous nutrient input to the ECS, previous research has reported that the Changjiang River (Yangtze River) transports thousands of tons of pollutants, such as heavy metals and persistent organic pollutants, including hydrocarbons (Lü and Zhai, 2005), pesticides, and PAHs (Guo et al., 2006; Feng et al., 2007; Müller et al., 2008; Deng et al., 2013) to the ECS per year. These PAHs discharged to the ECS may be easily accumulated in marine animals inhabiting the ECS through feeding links. Due to the fact that fish often migrate in response to their food sources, it is difficult to collect representative fish samples in their definite distribution areas. Instead of using wild fish species for the investigation of PAHs pollution in the ECS, here we use zooplankton for conducting such an investigation. Zooplankton species are lower trophic-level animals and typically move with ocean currents. To better understand how PAHs are distributed in zooplankton in the ECS, we investigated zooplankton PAHs concentrations in the ECS, with special emphasis on the effects of salinity (i.e., density) fronts.

2. Materials and methods A total of 32 hydrographic stations along several transects on the ECS shelf were conducted by the R/V Ocean Researcher I from April 29 to May 10, 2009 (Fig. 1). Temperature, salinity, and density were recorded using a Seabird SBE 911 plus a conductivity– temperature–depth (CTD) profiler. Concentrations of nitrate were measured according to Shih et al. (2013). The concentrations of chlorophyll-a (chl-a) in the surface layer (2 m) were determined according to Chen et al. (2013b). In brief, the chl-a samples were collected by filtering 500–2000 ml of seawater through a GF/F filter and stored at 20 °C until analysis. Chl-a on the GF/F filter was then extracted by acetone and determined according to standard procedures using a Turner Designs 10-AU-005 fluorometer by the non-acidification method (Chen et al., 2013b). The abundance of zooplankton in the surface layer was determined by collecting zooplankton with a standard zooplankton net (200 lm) towing in the surface layer for about 10–20 min. Prior to the analysis of PAHs, a small number of zooplankton samples were filtered for calculating the dry weight of zooplankton. The zooplankton sample was cleaned by separating it from possible micro-debris artifacts, as follows. The large visible non-zooplankton particles were picked out first and the rest of zooplankton samples with some seawater were stored at 20 °C until analysis (Hung and Gong, 2010). Towed zooplankton samples were defrosted and centrifuged (4000 rpm) at 4 °C for 15 min. The supernatant was discarded to remove microdebris. As mentioned earlier, the zooplankton net was used to collect zooplankton in the surface layer. If some micro-debris were collected with zooplankton in our samples, these tiny micro-debris should be in the supernatant after high-speed centrifugation. Therefore, we believe that almost all the micro-debris was removed after this procedure. After centrifugation, zooplankton were freeze-dried and weighed. Procedures for sample extraction, preparation, and analysis for PAHs in zooplankton were adapted

Fig. 1. Sampling locations for hydrography (solid black circles) in the East China Sea. CDW: Changjiang Diluted Water; KW: Kuroshio Water; TCWW: Taiwan Current Warm Water; YSW: Yellow Sea Water. Black dashed lines indicate isopycnic lines (S = salinity). This figure is modified from Fig. 1 of Hung et al. (2011). The blue dashed line represents the boundary of the Kuroshio. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Please cite this article in press as: Hung, C.-C., et al. Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.045

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from previous studies (Ko and Baker, 1995, 2004). Four perdeuterated PAHs (naphthalene-d8, fluorine-d10, fluoranthene-d10, and perylene-d12) were added to each sample prior to extraction as surrogates to assess the overall procedural recovery. Averaged recoveries in all zooplankton samples were 46 ± 10%, 64 ± 11%, 79 ± 18%, and 62 ± 11% for naphthalene-d8, fluorine-d10, fluoranthene-d10, and perylene-d12, respectively, while total PAH concentrations were not corrected for surrogate recoveries. Each freeze-dried sample was mixed with anhydrous sodium sulfate, ground with mortar, and pestled to obtain a dry powder. The powdered mass was then extracted with dichloromethane using an ASE 200 extractor (Dionex, Salt Lake City, UT, USA). The extracted volume was reduced to 1.5 ml using a rotary evaporator and then fractionated through an alumina oxide column to remove polar interferences using 35 ml of petroleum ether. The extract was concentrated to 5 ml by rotary evaporation and transferred to a pre-combusted, glass test tube. The extract volume was further reduced to 1 ml using a purified nitrogen stream and sealed in an amber vial for GC-MS analysis. The sample analysis was performed by a Varian 3800GC/Saturn 4000 ion trap mass spectrometer (Varian, Walnut Creek, CA, USA) operated in the ion-monitoring mode. Prior to the analysis, a mixture of perdeuterated PAHs, including phenanthrene-d10, benzo(a)anthracene-d10, benzo(a)pyrene-d12, and benzo(g,h,i)perylene-d12, was added immediately to each extract as an internal standard. Each PAH was identified by its retention time relative to the internal standards and quantified by comparing the integrated area of the molecular ion chromatogram to that of the internal standard (Ko and Baker, 1995, 2004). The detailed description about the PAH’s analysis can be found in Hung et al (2010). The concentrations of PAHs in zooplankton at 27 stations (excluding station 30 due to sample spilling) are expressed in two different units: ng g 1 (e.g., PAHs normalized by dry weight of zooplankton) and ng m 3 (e.g.,

PAH concentrations (ng g in seawater (g m 3)).

1

) normalized by zooplankton biomass

3. Results and discussion 3.1. Hydrographic setting and frontal zones in the ECS There are at least four main water masses (Fig. 1, CDW: Changjiang Diluted Water, TCWW: Taiwan Current Warm Water, KW: the Kuroshio Water, YS: Yellow Sea Water) in the ECS in April based on temperature and salinity distributions (Figs. 1 and 2 and Table 1). CDW is a mixture of Changjiang River runoff and shelf water with low salinity and high nutrient concentrations (Gong et al., 2003; Hung et al., 2013). YSW is mainly carried into the northern part of the ECS through the Chinese Coastal Current from the Yellow Sea (Ichikawa and Beardsley, 2002), showing moderate salinity, low temperature and low nutrient concentrations (Gong et al., 2003; Chou et al., 2009). TCWW enters the ECS from the Taiwan Strait with high temperature and high salinity (Gong et al, 2003), but its salinity is lower than that of the KW. The KW flows northeast along the shelf with high temperature, high salinity and low nutrient concentrations (Gong et al., 2003; Hung et al., 2009b). As a whole, the hydrographic setting in this survey in spring was similar to that reported for previous investigations (Gong et al., 2003; Chou et al., 2009). Fig. 2 shows contour maps of surface salinity, NO3 , Chl-a and plankton biomass in the ECS. Distributions of temperature, salinity, NO3 , Chl-a, and total PAHs along three transects (transect A: stations 19A, 29, 28, 27, and 26; transect B: stations 18, 17, 16, 15, and 14; transect C: stations 30, 31, 32 and 12) are shown in Fig. 3, respectively. Salinity distribution in the ECS indicates that the discharge of freshwater from the Changjiang River is located

Fig. 2. Sea surface salinity (A), NO3 concentration (B), Chl-a concentration (C) and plankton biomass (D) in the ECS. Black lines in panel A represent salinity (S) equal to 28, 30, and 32, respectively.

Please cite this article in press as: Hung, C.-C., et al. Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.045

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C.-C. Hung et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

Table 1 Depth, temperature (T), salinity (S), density (D), concentrations of nitrate (NO3 ), chlorophyll-a (chl-a), zooplankton biomass (biomass), zooplankton PAHs (Ra PAHs in dry weight and Rb PAHs in seawater volume) in the East China Sea. Sta.

Depth (m)

T (°C)

S

D (kg m

6 7 8 9 10 12 14 15 16 17 18 19 19A 20 21 22 23 24 26 27 28 29 30 31 32 34 35

31 88 109 121 155 106 107 95 69 71 45 37 32 52 50 65 80 102 95 92 60 60 33 83 97 107 78

17.9 21.9 21.6 19.7 20.8 23.0 20.0 19.8 18.6 18.0 18.4 16.8 18.5 15.7 17.1 17.2 16.5 20.2 19.9 18.1 17.7 17.8 18.4 17.7 18.8 25.3 23.4

29.8 34.1 34.2 33.9 34.3 34.5 34.0 33.7 32.1 31.3 29.0 29.6 29.8 32.5 32.7 33.0 33.0 34.4 34.4 33.7 33.6 29.6 27.9 31.1 33.1 34.1 34.2

21.3 23.5 23.7 24.0 24.0 23.6 24.0 23.8 22.9 22.5 20.5 21.4 21.2 23.9 23.8 24.0 24.1 24.2 24.4 24.3 24.3 21.2 19.8 22.3 23.6 22.6 23.2

3

)

NO3 (lM)

Chl-a (mg m

1.3 0.0 0.1 0.0 0.1 0.0 0.2 0.0 0.7 3.5 5.7 7.9 17.7 0.3 0.0 0.1 1.0 0.0 0.0 0.0 3.8 9.2 25.3 6.6 0.1 0.1 0.0

6.0 0.7 0.6 0.4 0.4 0.3 0.5 0.6 1.6 2.2 6.9 3.3 2.8 6.9 1.6 0.4 0.6 0.3 0.3 0.6 1.6 1.7 11.0 0.4 0.9 0.9 0.2

n.a.: Data not available. a Zooplankton PAHs in dry weight. b PAHs concentrations (ng g 1) normalized to zooplankton biomass (g m

3

3

)

Biomass (g m 0.391 0.031 0.155 0.045 0.068 0.026 0.029 0.004 0.008 0.148 0.703 0.272 0.280 0.268 0.025 0.171 0.138 0.273 0.041 0.068 0.078 0.142 0.041 3.204 0.279 0.034 0.033

3

)

Pa

PAHs (ng g

97 287 29 126 101 689 381 5384 909 115 144 113 116 61 127 148 50 64 173 66 54 130 n.a. 1093 203 53 218

1

)

Pb

PAHs (ng m

3

)

38 9 4 6 7 18 11 23 7 17 101 31 33 16 3 25 7 17 7 4 4 19 n.a. 3501 57 2 7

).

in the northeastern part of the study area. Several salinity fronts can be easily identified in the inner shelf and midshelf. The first front (salinity between <28 and >28), identified as the inner shelf front, appeared in the surface waters approximately 30–40 km offshore. The second front (salinity between 30 and 31), called the main front, was observed in the surface waters approximately 50–100 km offshore between stations 28–29, 17–18, and 30–31, respectively. This major front represents the boundary between the CDW and the midshelf water (e.g. the TCWW and the mixing water between the YSW and the TCWW). Across this front, hydrographic characteristics showed dramatic changes, with salinity increasing from about 29 to 31 (Fig. 3A) and with nitrate concentration decreasing from about 3–6 lM to around the detection limit (0.1 lM) (Fig. 3B). Surface Chl-a also dramatically changed across this front, decreasing by a factor of 1.5–10 from about 3– 10 mg m 3 to 0.5–1.0 mg m 3. The third front (salinity between 32 and 33), identified as the midshelf front, was located in the surface waters approximately 80–250 km offshore with salinity increasing from 32 to 33. These salinity fronts are mainly caused by a combination of freshwater discharge of the Changjiang River and forcing by northeasterly winds, as the observed wind direction during the sampling time in spring in the ECS was mainly from the northeast. In spring, the north-northeastern monsoon inhibits the northward excursion of the main plume of the Changjiang fresh water and forces the fresh plume to extend southwestward as a narrow band hugging the China coastline. Analogous hydrographic fronts in the ECS have been reported in the recent literature (Belkin et al., 2009; Chen, 2009). Distributions of nitrate and Chl-a concentrations along three transects mirrored the salinity distribution in the ECS (Fig. 3A–C). The observed dramatic changes of nitrate and Chl-a concentrations were correlated to hydrographic fronts at the three transects, even though the exact distributions of Chl-a concentrations and plankton biomass in the whole ECS may not totally coincide with

hydrographic fronts (Fig. 2C and D). Our results suggest that the variations in nitrate concentration are likely controlled by hydrography, while marine organism distributions in the study area (manifested in Chl-a and zooplankton) are more patchy and variable. Our interpretation is that the low concentrations of nitrate at some stations are a consequence of higher Chl-a concentration and thus, a passive (days to 1–2 weeks) result, while in other places, low nitrate concentration are unable to support much phytoplankton. Analogous uncoupling results between nitrate and Chl-a (or primary production) were also reported in the East China Sea (Hung et al., 2013). 3.2. Distribution of zooplankton PAHs in the ECS frontal zones Total concentrations of PAHs (as the sum of 50 compounds) in zooplankton ranged from 29 to 5384 ng g 1, showing a high spatial variation, with higher levels (>1000 ng g 1), when normalized to dry weight of zooplankton, found in coastal areas (Table 1 and Fig. 4). Surprisingly, the highest level of PAHs (5384 ng g 1, dry weight) was found in the the outer shelf region (i.e. station 15). We suggest that this could have been caused by low zooplankton weight (Table 1) as compared to other stations. The detailed data of PAHs at different stations are shown in Table 2 and the main compounds of PAHs in the zooplankton were phenanthrene (Phe), 2-methylanthracene, 4,6-dimethyldibenzothiophene, fluoranthene (Flu), pyrene (Pyr), Anthracene (An), Benzo (a)pyrene (BaP), Benzo(ghi)perylene (BghiP), and chrysene + triphenylene which are similar to previous investigations (Hung et al., 2011; Deng et al., 2013). These compounds have been reported in tributaries or the main stream of the Changjiang River and the estuary and/or coastal area of the ECS, indicating that pollution conditions of PAHs have existed in the ECS (Feng et al., 2007; Liu et al., 2008). This is probably due to the relatively large and rapid energy consumption in China, including 48% of coal, 11% of oil and

Please cite this article in press as: Hung, C.-C., et al. Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.045

C.-C. Hung et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

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Fig. 3. Water depth and the distribution of temperature (T), salinity (S), nitrate (NO3 ), Chl-a, and total PAHs in surface water along three transects (transect A: stations 19A, 29, 28, 27, and 26; transect B: stations 18, 17, 16, 15, and 14; transect C: stations 30, 31, 32 and 12) in the ECS. In transect C, PAHs data at station 30 are not available.

3.5% of natural gas of global energy consumption (BP, 2011). Undoubtedly, the eastern coastal provinces of China produced enormous PAHs in the world and these PAHs are easily be transported to the ECS. The distribution of PAHs in zooplankton may be related to other hydrographic parameters such as nutrient and Chl-a concentration. However, we did not find a pronounced correlation between PAHs and nutrient (and Chl-a) concentrations, indicating that nutrient and phytoplankton distributions could not help in the interpretion of the variations of PAHs concentrations in zooplankton in this study. Besides the effect of water masses, the high variation of PAHs in zooplankton was likely affected by different zooplankton species, growth stage (Lotufo, 1998) or lipid contents (Bruner et al., 1994). However, when compared to literature data on total PAHs concentrations in marine organisms (such as copepods and amphipod), the observed PAHs data in zooplankton in this study are in agreement with those documented elsewhere (Harris et al., 1977; Ko and Baker, 1995; Lotufo, 1998; Vigano et al., 2007). Due to patchiness in zooplankton abundance in surface waters (Table 1), we prefer to report abundance in ng m 3 (calculated as the product of PAH concentration in ng g 1 and abundance in g m 3), when discussing the distributions of total PAHs concentrations in the

frontal zones of the ECS. Total concentrations of zooplankton PAHs in the CDW ranged from 2 to 3500 ng m 3 (e.g. station 31), with the maximum PAHs at the front between the CDW and the midshelf waters (Fig. 3). In contrast, concentrations of PAHs in zooplankton in the mid-shelf and outer shelf waters (4.5–23.5 ng m 3) were significantly lower than those in the CDW. These results demonstrate the fact that PAHs in zooplankton can be highly concentrated in salinity frontal zones in the ECS, even though this it is not always the case. As mentioned above, the accumulation of PAHs in zooplankton not only depends on zooplankton species, but also on lipid content and body size (Bruner et al., 1994). We did not have zooplankton species data in this study, but it should be highly variable for zooplankton species in the ECS based on previous studies (Shih and Chiu, 1998; Wu et al., 2010). As mentioned in the method section, we used a standard zooplankton (200 lm) net to collect zooplankton, but the zooplankton samples might also contain some tiny marine plastic debris. Hirai et al. (2011) reported that plastic fragments on the sea surface are also absorbing organic pollutants, including PAHs. Because visible non-zooplankton particles were picked out prior to determination of PAHs, the effect of plastic debris on the data of zooplankton PAHs are likely not important. However, there is

Please cite this article in press as: Hung, C.-C., et al. Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.045

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no guarantee that our zooplankton samples were excluding all PAHs adsorbed to plastic debris. Thus, it might be worthy to conduct PAHs in tiny plastic debris (i.e. non visible plastic particles) in the future. 3.3. Sources of zooplankton PAHs in the ECS frontal zones

Fig. 4. Total PAHs in zooplankton (A: dry weight; B: dry weight normalized to zooplankton biomass in seawater) in the ECS.

Table 2 Concentrations (ng g

Different molecular ratios such as An/178, Fl/(Fl + Py), Nap/FL and BaA/288 in sediments have been used to diagnose possible sources of PAHs from pyrogenic or petrogenic sources (Gotz et al., 1998; Soclo et al., 2000; Kavouras et al., 2001; Yunker et al., 2002; Fang et al., 2003, 2007; Doong and Lin, 2004; Li et al., 2006; Hung et al., 2011). In this study, the index of PAH isomer ratios was implemented for plankton samples by assuming the particulate-dissolved partitioning and biodegradation of each PAH compound would be constant at all sampling sites. Ratios of An/178 in the collected samples at stations 7, 15, 24, 34, 35 were higher than 0.1, clearly suggesting terrestrial sources from the combustion of grass/wood/coal (Fig. 5). The ratios (An/178 < 0.1 and BaA/288 < 0.2) at stations 20, 21, 22 and23 suggest that the high PAH concentrations at these stations may be due to occasional petroleum contamination (or accidently discharge) from ships or fishing boats. Ratios of Fl/(Fl + Py) > 0.5 at stations 6, 19, 26 may suggest a combination of combustion and petroleum in some zooplankton in the ECS (Fig. 4B). Besides terrestrial or ship sources, long-range aeolian transport may also contribute PAHs to zooplankton in the ECS. According to the literature (Tamamura et al., 2007; Cheng et al., 2013; Lai et al., 2014), atmospheric currents mainly originate from the areas of northern China in winter and its adjacent areas. In fact, recent reports provide evidence that Asian dust storms indeed carry aerosol particles containing inorganic and organic nutrients and persistent organic pollutants

1

) of individual PAHs in surface zooplankton in the ECS.

PAH compound/Station

6

7

8

9

10

12

14

15

16

17

18

19

19A

2-Methylnaphthalene 1-Methylnaphthalene 2,6-Dimethylnaphthalene 1,3-Dimethylnaphthalene 1,6-Dimethylnaphthalene 1,4-Dimethylnaphthalene 1,5-Dimethylnaphthalene 1,2-Dimethylnaphthalene 1,8-Dimethylnaphthalene 2,3,5-Trimethylnaphthalene Acenaphthylene Acenaphthene Fluorene 1-Methylfluorene Dibenzothiophene Phenanthrene Anthracene 2-Methylphenanthrene 2-Methylanthracene 4,5-Methylenephenanthrene 1-Methylanthracene 1-Methylphenanthrene 4,6-Dimethyldibenzothiophene 9-Methylanthracene 3,6-Dimethylphenanthrene 2,3-Dimethylanthracene 9,10-Dimethylanthracene Retene Fluoranthene Pyrene 2-Methylfluoranthene Benzo[a]fluorene

5.4 2.8 2.4 1.0 n.d. 5.2 n.d. 2.1 n.d. 1.3 0.4 1.2 4.0 3.2 2.4 10.2 1.3 4.7 6.6 n.d. 4.1 2.4 4.8 n.d. n.d. n.d. n.d. 2.2 6.1 3.9 0.8 2.3

9.1 5.0 2.6 6.3 2.5 2.2 1.3 n.d. n.d. 8.1 1.8 1.5 9.4 12.3 9.5 30.0 6.5 30.3 32.2 7.0 4.0 19.9 31.8 0.7 5.7 2.6 n.d. n.d. 7.1 10.5 1.3 2.6

2.6 0.4 1.7 n.d. 0.5 n.d. n.d. n.d. n.d. 0.2 n.d. 0.8 1.4 0.8 n.d. 3.3 n.d 1.0 2.2 n.d. 2.0 0.5 1.8 n.d. n.d. n.d. n.d. n.d. 2.5 1.0 0.3 n.d.

10.3 5.4 1.0 2.0 1.1 1.4 n.d. 1.2 n.d. 5.4 1.3 3.3 10.3 3.7 4.0 30.0 1.9 3.2 7.8 n.d. 5.1 3.4 5.4 0.6 n.d. n.d. n.d. 1.6 6.9 1.7 0.2 n.d.

7.1 2.8 3.0 1.6 0.4 2.5 n.d. 1.7 n.d. 0.7 n.d. n.d. 5.8 4.9 2.7 12.7 1.6 2.6 4.6 n.d. 3.1 2.1 4.2 n.d. n.d. n.d. n.d. 0.8 5.0 1.5 0.1 1.7

49.0 35.6 9.5 27.4 8.8 7.5 4.4 8.5 n.d. 12.8 1.8 4.2 14.2 25.8 33.1 88.2 10.4 70.2 77.9 n.d. 46.4 35.6 47.3 1.2 8.2 0.1 n.d. 2.4 8.1 12.0 1.1 1.7

16.4 7.1 9.5 7.6 4.0 11.6 12.9 2.3 n.d. 3.9 1.5 4.1 15.5 7.6 9.6 36.0 4.7 19.9 23.6 n.d. 20.8 11.1 21.4 1.2 5.1 n.d. n.d. 4.9 11.6 14.5 3.2 5.8

62.5 50.6 170.5 208.8 95.0 58.7 45.9 52.5 n.d. 114.4 33.3 24.0 90.7 128.1 126.5 368.4 103.2 343.0 384.0 7.7 373.2 214.8 369.4 12.2 176.1 23.5 n.d. 25.7 230.1 424.6 50.0 148.8

20.3 11.1 6.6 4.3 2.3 5.6 n.d. 2.4 n.d. 2.3 n.d. 2.8 6.2 5.9 6.9 31.9 3.4 53.0 87.0 n.d. 56.6 40.4 78.6 n.d. 37.5 n.d. n.d. 18.8 13.9 42.4 20.7 21.5

2.3 n.d. 1.7 2.6 n.d. 2.0 n.d. n.d. n.d. 2.1 n.d. 1.6 4.8 8.6 3.4 19.8 n.d. 5.8 9.5 n.d. 8.1 3.3 8.1 1.3 n.d. n.d. n.d. 1.3 9.1 2.3 1.1 1.9

2.8 n.d. 1.7 n.d. n.d. 0.2 n.d. n.d. n.d. 0.8 n.d. 0.9 4.0 2.2 3.7 12.8 1.4 16.3 23.1 n.d. 11.3 9.3 11.7 n.d. 1.7 n.d. n.d. 2.2 4.6 5.2 1.6 0.8

6.6 2.1 2.6 n.d. n.d. n.d. n.d. 0.7 n.d. 0.7 n.d. 1.8 4.2 5.5 2.3 9.6 1.3 3.6 7.0 n.d. 3.3 3.0 3.5 n.d. n.d. n.d. n.d. 0.1 6.8 1.8 0.5 1.6

5.9 1.0 3.4 1.1 0.8 3.7 n.d. n.d. n.d. 2.2 0.9 1.0 4.0 1.8 0.6 6.9 0.2 5.2 7.2 n.d. 3.7 2.3 5.8 2.4 n.d. n.d. n.d. n.d. 8.1 5.9 1.5 3.6

Please cite this article in press as: Hung, C.-C., et al. Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.045

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C.-C. Hung et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx Table 2 (continued) PAH compound/Station

6

7

8

9

10

12

14

15

16

17

18

19

19A

Benzo[b]fluorene 1-Methylpyrene Benzo[a]anthracene Chrysene+Triphenylene 1-Methylbenzo[a]anthracene 4/6-Methylchrysene 3,9-Dimethylbenzo[a]anthracene Benzo[b]fluoranthene Benzo[k]fluoranthene Benzo[e]pyrene Benzo[a]pyrene Perylene 10-Methylbenzo[a]pyrene 7,10-Dimethylbenzo[a]pyrene Dibenzo[a,h]anthracene Indeno[1,2,3-c,d]pyrene Benzo[g,h,i]perylene Coronene PAH compound/Station 2-Methylnaphthalene 1-Methylnaphthalene 2,6-Dimethylnaphthalene 1,3-Dimethylnaphthalene 1,6-Dimethylnaphthalene 1,4-Dimethylnaphthalene 1,5-Dimethylnaphthalene 1,2-Dimethylnaphthalene 1,8-Dimethylnaphthalene 2,3,5-Trimethylnaphthalene Acenaphthylene Acenaphthene Fluorene 1-Methylfluorene Dibenzothiophene Phenanthrene Anthracene 2-Methylphenanthrene 2-Methylanthracene 4,5-Methylenephenanthrene 1-Methylanthracene 1-Methylphenanthrene 4,6-Dimethyldibenzothiophene 9-Methylanthracene 3,6-Dimethylphenanthrene 2,3-Dimethylanthracene 9,10-Dimethylanthracene Retene Fluoranthene Pyrene 2-Methylfluoranthene Benzo[a]fluorene Benzo[b]fluorene 1-Methylpyrene Benzo[a]anthracene Chrysene+Triphenylene 1-Methylbenzo[a]anthracene 4/6-Methylchrysene 3,9-Dimethylbenzo[a]anthracene Benzo[b]fluoranthene Benzo[k]fluoranthene Benzo[e]pyrene Benzo[a]pyrene Perylene 10-Methylbenzo[a]pyrene 7,10-Dimethylbenzo[a]pyrene Dibenzo[a,h]anthracene Indeno[1,2,3-c,d]pyrene Benzo[g,h,i]perylene Coronene

1.2 0.7 1.8 6.1 0.3 0.8 1.7 1.2 0.7 n.d. n.d. 0.7 n.d. n.d. n.d. n.d. n.d. 0.9 20 2.6 1.0 1.9 n.d. n.d. 2.5 n.d. 0.8 n.d. 1.4 0.7 n.d. 4.2 4.4 1.6 8.3 0.6 3.0 3.2 0.1 2.2 2.1 2.4 0.7 n.d. n.d. n.d. 0.2 4.2 0.6 n.d. 0.2 0.7 0.1 4.2 1.6 0.7 n.d. n.d. 0.3 n.d. n.d n.d. n.d. n.d. 4.2 0.1 0.6 n.d. n.d.

1.6 3.1 2.2 3.9 2.9 n.d. n.d. 2.3 0.4 n.d. n.d. 3.5 n.d. 1.8 n.d. 0.3 1.1 0.7 21 14.2 10.0 1.4 4.4 0.7 3.8 n.d. 1.9 n.d. 2.6 n.d. 2.8 6.9 4.8 4.1 23.2 1.2 3.8 5.5 n.d. 4.0 2.8 6.7 n.d. n.d. n.d. n.d. 1.3 4.0 2.3 0.3 0.4 n.d. 0.2 n.d. 1.2 1.6 n.d. n.d. 0.8 n.d. n.d. n.d. n.d. n.d. 10.0 n.d. n.d. n.d. n.d.

n.d. n.d. n.d. 1.1 0.5 n.d. n.d. 1.0 0.4 n.d. n.d. 1.5 n.d. 1.1 n.d. n.d. n.d. n.d. 22 6.5 2.7 2.8 0.5 0.1 n.d. n.d. 0.4 n.d. 0.2 0.1 1.0 2.8 3.4 0.2 5.0 0.2 6.2 6.4 n.d. 2.7 2.9 3.2 n.d. n.d. n.d. n.d. 1.6 4.3 3.3 1.8 2.1 n.d. 4.5 2.2 5.1 0.2 2.7 1.6 0.6 n.d. n.d. n.d. 0.3 7.1 63.3 n.d. n.d. n.d. 0.3

0.3 0.1 n.d. 1.7 0.1 0.6 n.d. 2.3 1.0 n.d. n.d. 0.2 0.8 0.6 n.d. n.d. n.d. 0.3 23 1.0 n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. n.d. 0.6 n.d. 3.9 0.8 2.5 9.8 0.1 1.1 2.4 1.2 2.3 1.1 3.6 n.d. n.d. n.d. n.d. n.d. 6.4 0.5 0.2 0.3 0.3 n.d. 0.4 3.1 n.d. 0.3 3.3 n.d. 0.8 n.d. n.d. 0.1 3.6 n.a n.a n.a n.a n.a

0.1 1.9 n.d. 0.6 0.2 0.3 n.d. 1.6 0.4 n.d. n.d. 0.5 n.d. 20.7 0.4 n.d. n.d. 0.5 24 3.0 2.1 3.5 3.9 1.5 1.0 0.9 1.1 n.d. 1.7 0.6 0.6 2.1 2.2 1.8 7.2 1.3 3.4 4.4 n.d. 3.1 1.9 2.9 n.d. 0.2 0.1 n.d. 0.1 2.0 2.6 0.2 0.4 0.3 0.3 0.4 0.6 n.d. n.d. 0.1 0.5 0.3 n.d. n.d. 0.1 0.9 4.3 n.d. n.d. n.d. n.d.

1.3 4.1 1.8 1.6 2.9 0.6 n.d. 3.3 0.2 n.d. n.d. 0.4 5.7 10.1 n.d. n.d. 2.3 1.5 26 36.5 31.0 7.1 9.1 2.1 3.2 n.d. 1.9 n.d. 2.0 0.4 1.2 3.8 4.8 3.5 15.0 n.d. 3.8 8.6 n.d. 5.9 3.3 5.9 n.d. n.d. 0.9 n.d. n.d. 4.9 2.6 0.6 1.1 0.1 0.9 0.9 1.7 3.8 1.1 0.2 0.8 0.1 n.d. n.d. 0.1 0.1 3.2 n.d. n.d. 1.0 0.3

1.7 9.1 6.6 12.7 2.0 8.8 7.0 4.5 1.9 11.1 n.d. 1.3 1.4 4.3 1.3 0.9 6.0 2.4 27 5.8 2.1 3.2 0.7 0.9 3.7 n.d. 2.3 n.d. 2.6 n.d. n.d. 3.2 1.1 2.6 10.6 n.d. 2.4 4.2 n.d. 4.1 2.4 3.8 n.d. n.d. n.d. n.d. 0.5 5.2 0.8 0.2 0.1 n.d. n.d. n.d. 1.7 n.d. n.d. n.d. 0.2 n.d. n.d. n.d. n.d. n.d. 1.5 n.d. n.d. n.d. n.d.

67.4 140.8 96.7 97.6 23.7 16.1 4.3 95.7 30.9 39.0 21.0 13.6 7.8 32.5 n.d. 55.7 84.0 40.4 28 2.9 0.4 1.3 n.d. n.d. 1.0 n.d. 3.0 n.d. 0.3 n.d. n.d. 1.8 1.3 1.3 6.2 n.d. 3.1 5.1 n.d. 3.6 2.1 5.6 n.d. n.d. n.d. n.d. 0.9 5.2 1.5 0.1 0.6 n.d. 0.6 n.d. 3.7 0.8 0.0 n.d. 0.3 n.d. n.d. n.d. 0.9 0.1 0.3 n.d. n.d. n.d. n.d.

6.9 51.1 22.5 67.3 9.9 37.1 34.9 20.2 4.3 31.7 n.d. 0.8 5.0 2.9 3.4 2.1 20.6 6.4 29 14.1 10.9 0.8 5.2 1.3 6.6 n.d. 2.7 n.d. 2.9 n.d. n.d. 1.0 5.3 2.9 16.6 n.d. 7.1 9.8 n.d. 4.9 4.5 4.8 0.2 n.d. n.d. n.d. 0.5 5.1 2.4 0.3 1.0 0.1 0.2 n.d. 2.0 n.d. 0.1 n.d. 1.3 0.5 n.d. n.d. 1.9 0.7 11.4 n.d. 0.3 0.8 0.2

0.3 0.2 0.9 5.3 2.5 0.4 3.1 0.5 0.5 n.d. n.d. 0.1 n.d. n.d. n.d. n.d. n.d. 0.6 31 17.7 9.4 1.9 5.7 2.4 4.0 n.d. 1.8 n.d. 9.8 0.5 2.3 11.9 26.8 61.4 170.3 9.6 168.8 173.9 n.d. 103.8 67.1 90.9 n.d. 23.0 5.6 n.d. 5.9 10.4 18.1 3.9 3.9 0.7 4.7 n.d. 19.7 9.2 7.6 4.0 7.3 n.d. n.d. n.d. 0.1 2.1 21.4 n.d. n.d. 4.8 n.d.

0.7 2.1 1.7 6.4 7.2 1.9 1.5 1.0 1.1 n.d. n.d. 0.6 0.5 n.d. n.d. 1.1 n.d. 0.1 32 15.8 9.5 7.1 7.0 2.7 1.9 3.3 2.5 n.d. 5.3 0.1 n.d. 10.2 7.3 7.0 28.2 2.9 15.6 14.5 n.d. 12.2 9.1 14.0 n.d. 0.1 n.d. n.d. 1.3 7.3 4.6 0.5 0.6 0.3 0.8 n.d. 4.4 3.5 0.8 0.4 1.4 n.d. n.d. n.d. 0.1 n.d. n.d. n.d. 0.1 0.7 n.d.

0.6 0.7 1.2 5.1 0.1 0.2 n.d. 1.7 0.2 n.d. n.d. 1.3 n.d. 31.3 n.d. 0.8 n.d. 0.8 34 11.2 6.1 3.2 1.7 0.5 2.2 n.d. 0.4 n.d. 0.4 n.d. 1.6 1.0 2.0 0.5 2.2 0.7 1.5 2.3 n.d. 3.3 0.2 3.5 0.1 n.d. n.d. n.d. 0.5 0.6 0.8 n.d. 0.3 n.d. n.d. n.d. n.d. n.d. 0.1 n.d. n.d. 0.1 n.d. n.d. n.d. n.d. 4.3 0.9 0.1 n.d. 0.2

1.7 1.9 5.7 9.6 7.7 1.6 1.3 3.9 0.2 n.d. n.d. 2.1 0.8 n.d. n.d. n.d. n.d. 0.8 35 70.1 44.8 4.0 13.4 3.2 6.8 n.d. 2.8 n.d. 1.1 0.1 0.4 0.9 3.6 1.4 1.6 1.1 3.0 4.8 n.d. 2.8 2.1 4.4 n.d. n.d. n.d. n.d. 0.3 1.1 2.9 0.2 0.5 n.d. 0.4 n.d. 1.2 n.d. 0.1 n.d. 1.1 0.3 n.d. n.d. 0.8 1.0 12.2 0.3 0.6 21.7 0.8

n.d.: Not detectable.

(including PAHs, pesticides and PCBs) in northern China, the Yellow Sea, the East China Sea and in Japan (Tang et al., 2005; Lammel et al., 2007; Tamamura et al., 2007; Hung et al., 2009b; Chen et al., 2010), but it is difficult to quantitatively evaluate the

flux of PAHs. The observed results suggest that petroleum supply is likely an important PAH source in the study area. The second key source is a mixed source of petroleum and combustion of grass/wood/coal. This is supported by previous investigations that

Please cite this article in press as: Hung, C.-C., et al. Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.045

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C.-C. Hung et al. / Marine Pollution Bulletin xxx (2014) xxx–xxx

Fig. 5. Relationship between (a) An/178 (anthracene/(anthracene + phenanthrene)) and Fl/Fl + Py (fluoranthene/(fluoranthene + pyrene)), (b) BaA/288 (benzo[a]anthracene/ (benzo[a]anthracene + chrysene/triphenylene)) and Fl/Fl + Py in surface zooplankton in the ECS.

reported that combustion and terrestrial discharge are the two major sources of sedimentary PAHs in the ECS (Feng et al., 2007; Hung et al., 2011). 3.4. Implication of zooplankton PAHs in frontal zones affecting marine ecosystems Frontal zones are important nursery, feeding, and fishing grounds (Nakata et al., 2000; Kasai et al., 2002, and references in Belkin et al., 2009). According to Landrum et al. (1992), PAHs can be taken up by marine organisms through direct adsorption of freely dissolved chemicals and/or direct contact and ingestion of sediment particles. We could not distinguish the exact mechanism, which resulted in elevated PAHs concentrations in zooplankton in our study area, but the distribution patterns of Chl-a concentrations and zooplankton abundance in the ECS along the three transects were similar to those of PAHs (Fig. 3A–C). The results thus strongly suggest that zooplankton accumulate PAHs via food chain magnification and/or absorption of PAHs. Because most of PAHs are hydrophobic, they can be easily incorporated by phytoplankton (Bruner et al., 1994; Vigano et al., 2007). Ko et al. (2012) reported that many organic pollutants (including PCBs and organo-chlorine pesticides) can be absorbed quickly in phytoplankton culture experiments. In other words, PAHs in/on phytoplankton can be taken up by zooplankton and accumulated in zooplankton. These higher levels of PAHs in zooplankton may be transported to higher eutrophic levels of marine organisms through the marine food web because the coastal hydrographic frontal zones are important fish nursery grounds. Additionally, the fecal pellets produced by PAH-contaminated zooplankton may carry PAHs to greater depths. Recently, Tanabe et al. (2005) reported that deepsea organisms in the ECS contained organo-chlorine pollutants and suggested that organic pollutants in deep-sea organisms may be from coastal regions via horizontal transport. We did not measure the content of PAHs in fecal pellets generated by zooplankton, but Wang et al. (2001) reported that the fecal pellets produced by Capitella in sediments appear to contain more PAHs than organic matter associated with clay minerals. Additionally, Prahl and Carpenter (1979) suggested that the zooplankton fecal pellets, collected in Dabob Bay [a bay adjacent to Puget Sound in Washington, USA] may control PAH removal to sediments. Furthermore, Cailleaud et al. (2007) reported that copepods could have a high accumulation factor for PAHs. Our results imply that PAHs can be highly accumulated by zooplankton in oceanic frontal zones and transported PAHs to deeper waters. Thus, PAH-contaminated zooplankton may also pose a risk to their predators.

4. Conclusions Based on field observations of zooplankton PAHs and hydrographic data in the ECS, we conclude that the concentration of zooplankton PAHs changes dramatically from the inner shelf (17–3500 ng m 3) to the outer shelf (4.5–23.5 ng m 3) across salinity fronts in the ECS. Thus, PAHs are strongly accumulated in zooplankton at the salinity front between inner and middle shelves. The dramatic variation of zooplankton PAHs might require further investigations. It is suggested that the PAH-contaminated zooplankton may cause increased risk when PAHs are further biomagnified in the marine food web. Acknowledgements We are grateful for the assistance of the crew of the R/V Ocean Researcher I in collecting samples. We also thank an anonymous reviewer and the Chief Editor for giving constructive comments that improved the paper. This research was supported by grants from the Top University Program and the Ministry of Science and Technology of Taiwan (NSC101-2611-M-110-015-MY3, NSC1012116-M-110-001).

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Please cite this article in press as: Hung, C.-C., et al. Increased zooplankton PAH concentrations across hydrographic fronts in the East China Sea. Mar. Pollut. Bull. (2014), http://dx.doi.org/10.1016/j.marpolbul.2014.03.045