Trace metals in seawater and copepods in the ocean outfall area off the northern Taiwan coast

MARINE ENVIRONMENTAL RESEARCH Marine Environmental Research 61 (2006) 224–243 www.elsevier.com/locate/marenvrev

Trace metals in seawater and copepods in the ocean outfall area off the northern Taiwan coast Tien-Hsi Fang a

a,* ,

Jiang-Shiou Hwang b, Shih-Hui Hsiao b, Hung-Yu Chen a

Department of Marine Environmental Informatics, National Taiwan Ocean University, Keelung 20224, Taiwan, ROC b Institute of Marine Biology, National Taiwan Ocean University, Keelung, Taiwan

Received 20 June 2004; received in revised form 21 September 2005; accepted 16 October 2005

Abstract The distribution, partitioning and concentrations of trace metals (Cd, Cr, Cu, Fe, Mn, Pb and Zn) in seawater, including dissolved and particulate phases, and in copepods in the ocean outfall area off the northern coast of Taiwan were investigated. Normalization of metal concentrations to the background metal concentration to yield relative enrichment factors (EF), which were used to evaluate the contamination of dissolved and particulate trace metals in seawater around the ocean outfall. The EF results indicated that the outfall area was significantly contaminated by dissolved Fe and Zn, and by particulate Fe, Cr, Cu, Pb and Zn. In addition, most trace metals were chiefly in the particulate phase. The average percentage of total metal concentrations (dissolved plus particulate phases) bound by suspended particulate matter followed the sequence Al(95%) = Mn(95%) > Pb(88%) > Cu(86%) > Fe(72%) > Zn(32%) > Cr(17.5%) > Cd(3.4%). Therefore, metal contamination is better evaluated in solid phase than in the dissolved phase. The concentration ranges of trace metals in the copepods, Temora turbinata, Oncaea venusta and Euchaeta rimana, near the outfall were: Cd, 0.23–1.81 lg g 1; Cr, 16.5–195 lg g 1; Cu, 14– 160 lg g 1; Fe, 256–7255 lg g 1; Mn, 5.5–80.8 lg g 1; Pb, 2.6–56.2 lg g 1; Zn, 132–3891 lg g 1; and Al, 0.21–1.13%. Aluminum, and probably Fe, seemed to be the major elements in copepods. The concentrations of trace metals in copepods, especially Temora turbinata, near the outfall were generally higher than those obtained in the background station. The mean increase in bioconcentration factor of metals in copepods ranged from 4 to 7 and followed the sequence Al(6.4) > Cu(6.2) > Fe(6.0) > Zn(5.7) > Pb(5.6) > Cr(5.5) > Cd(5.1) > Mn(4.7). Therefore, marine copepods in the *

Corresponding author. Tel.: +886 2 24622192x6343; fax: +886 2 4627674. E-mail address: [email protected] (T.-H. Fang).

0141-1136/$ - see front matter
2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.marenvres.2005.10.002

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waters of northern Taiwan can accumulate trace metals over background concentrations and act as contamination indicators.
2005 Elsevier Ltd. All rights reserved. Keywords: Trace metals; Copepod; Ocean outfall; Bioconcentration; Enrichment factor

1. Introduction Estuarine and coastal environments are contaminated by human waste containing elevated concentrations of nutrients, organic pollutants, trace metals, and radionuclides (Kennish, 1999; Clark, 2001). Some chemicals are highly toxic and persistent, and have a strong tendency to become concentrated in marine food webs. The pollution of coastal zones near metropolitan areas, by these anthropogenic wastes is due to the large coastal human population and the enormous amounts of sewage discharged in coastal waters (Bay, Zeng, Lorenson, Tran, & Alexander, 2003; Bothner, Casso, Rendigs, & Lamothe, 2002; Gonzalez, Pomares, Ramirez, & Torres, 1999; Matthai, Birth, & Bickford, 2002; Sadiq, 2002). Even so, ocean outfalls occur in all coastal cities because it is believed that oceans have a great capacity to assimilate sewage (Koop & Hutchings, 1996). Taipei city, located in northern Taiwan, is its largest city and the capital of Taiwan. Six million people, over a quarter of TaiwanÕs population, live in the metropolitan area. Due to economic expansion and no regulation of wastewater discharges during the last three decades, the estuaries of northern Taiwan have received untreated domestic discharge and both treated and untreated industrial effluent from its tributaries. Thus, the inshore environment has been obviously polluted by organic materials, nutrients, and trace metals (Fang, 2000; Fang & Lin, 2002; Jeng & Han, 1994). In order to improve the water quality and to better manage the inshore environment, the Taipei city government started to construct a domestic wastewater treatment plant in the 1990s. The primarily treated wastewater was designed to be discharged along the coast through the ocean outfall area. This ocean outfall area was the first ever constructed in Taiwan and was commissioned in June, 1998. It has long been recognized that trace metals, such as Cu, Cr, Pb, and Zn, in marine environments are highly persistent and can be toxic in trace amounts (Bothner et al., 2002; Langston, 1990; Long, Macdonald, Smith, & Calder, 1995). Thus, the distribution and concentrations of trace metals near the ocean outfall should be assessed to understand the nature and extent of anthropogenic influence, and to determine possible toxic effects (Matthai et al., 2002). Because of their wide geographic distribution, their trophic position, their rapid turnover, huge biomass, potential role as good indicators of the minimal lethal concentration of metals (Barka, Pavillon, & Amiard, 2001), and their great capacity to accumulate trace metals (Kahle & Zauke, 2002; Wang & Fisher, 1998), copepods are increasingly used as trace metals biomonitors in marine environments (Barka et al., 2001; Kahle & Zauke, 2002, 2003; Ritterhoff & Zauke, 1997). Taiwan is an island located in the tropical to sub-tropical western Pacific. The northern shelf of Taiwan is an extremely dynamic oceanic region where the Kuroshio Branch Current intrudes and the northward-flowing Taiwan Strait Current passes. The Kuroshio Branch Current runs into the continental shelf-break off the northeast Taiwan and forms a year-round upwelling (Liu et al., 1992). Many studies have shown that copepods were abundant in the northern coast of Taiwan. More than 116 species of copepods belonging

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to 47 genera and 25 families were identified and the amounts of copepods ranged from 100 to 200 inds m 3 in the coastal seawater and decreased to 20–50 inds m 3 in the central northern Taiwan Strait (Hsieh & Chiu, 1998; Hsieh & Chiu, 2002; Hwang, Chen, & Wong, 1998; Lo, Shih, & Hwang, 2004). These studies indicate that the most abundant species of copepods were Temora turbinata, Paracalanus parvus, Canthocalanus pauper, Acrocalanus gibber and Euchaeta sp. This study presents the preliminary results on trace metals in copepods and in seawater around the ocean outfall area off the northern Taiwan coast. The aim of this study is to understand the trace metal pollution near the ocean outfall area through analyses of trace metals in seawater and in copepods. 2. Materials and methods 2.1. Study area The Bali wastewater primary treatment plant is located at Bali, near the Tanshui estuary, and has a maximum treatment capacity of 1.32 · 106 m3 d 1 (CMD). Treated wastewater is discharged approximately 6.6 km offshore via an ocean outfall pipe (Fig. 1). In 1999, the mean daily discharge was 5.29 · 105 CMD and the mean concentration of particles and pH of the effluents were 70 mg L 1 and 7.06, respectively (Department of Publics Sewerage Systems Report, 2001). Dissolved oxygen concentration near the outfall in 1999 ranged from 3.4 to 6.1 ml L 1, with a mean value of 4.8 ml L 1, approaching saturation. In addition, the maximum salinity recorded near the ocean outfall was generally less than 33.6, suggesting that dilution of the ocean outfall discharge by adjacent seawater was about 150-fold (Department of Publics Sewerage Systems Report, 2001). The Tanshui River is formed by the confluence of Tahan Stream, Hsintein Stream and the Keelung River. Downstream portions of all three tributaries form the Tanshui estuarine

Fig. 1. Map of the study area with sampling stations in the ocean outfall area (stations 1–13) and at the background locations (B1 and B2), northern Taiwan. Bali WTP stands for ‘‘Bali wastewater treatment plant’’. The dash lines in figure are depth contour (m).

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system, located on the outskirts of Taipei, which is the largest estuary in northern Taiwan. It discharges into the northern Taiwan Strait. The total length of the Tanshui River system is 159 km and its drainage area is 2726 km2. The mean annual river discharge and suspended particulate matter transport over the last 40 years have been approximately 7044 · 106 m3 y 1 and 11.45 · 106 t y 1, respectively (Hydrological Year Book of Taiwan, 1999). The river system is sufficiently narrow that there is no significant wind-induced current in the river. The major forcing mechanisms for flow are tidal at river mouth and river discharge upstream. Semi-diurnal tides are the principal tidal components, with a mean tidal range of 2.22 m and a spring tidal range of 3.1 m. In addition, the barotropic flow caused by density difference is another important transport mechanism in the Tanshui River estuary system (Liu, Hsu, Kuo, & Kuo, 2001). Northern Taiwan is bounded by the Taiwan Strait in the west, the Kuroshio in the east and the East China Sea in the north. As northern Taiwan lies on the path of the northeast monsoon, Kuroshio Water occasionally makes an intrusion onto the northern Taiwan shelf, forming a cold dome of upwelled subsurface water along the eastern edge of the shelf (Liu et al., 1992). It is well documented that Taiwan Strait Water is made up of three different water masses from the East China Sea, the South China Sea and the Kuroshio, respectively. The flow pattern in the Taiwan Strait is dominated by the East Asian monsoon and generally has a northward direction (Wang and Chern, 1988). Thus, water masses in northern Taiwan are significantly influenced by the seasonal intrusion of the Kuroshio Water and by the northward flow of the Taiwan Strait Current. For these reasons, currents off northern Taiwan are complicated and not well understood (Liu, Peng, Shaw, & Shiah, 2003). 2.2. Sampling and analysis Water samples around the outfall were taken onboard the R/V Ocean Research-II on June 2–3, 2003. The sampling stations formed a square that encompassed the ocean outfall area (Fig. 1). For better understanding the influence of outfall discharge, water samples in surface (0 m), middle and bottom layer were collected at each of the stations using Go-Flo bottles mounted on a Rosette sampling assembly and were stored in acid-cleaned 1-L Nalgene low density polyethylene bottles (LDPE). Three layers of water samples at two reference stations, approximately 10 and 20 km away from the ocean outfall area, were also collected and were considered to represent background stations. The sampling depths of middle and bottom layers at each of the stations were not consistent because of the topographical variations. The LDPE bottles were rigorously cleaned by sequentially soaking them in a detergent solution and in a mixture consisting of 50% (v/v) hydrochloric acid and 50% (v/v) nitric acid, prior to use. In order to prevent adsorption of dissolved compounds on the inner walls of the bottles, samples were frozen immediately on board ship. Analytical procedures were carried out in a land-based laboratory. Full details of the sampling and pretreatment procedures are given elsewhere (Fang & Lin, 2002). Zooplankton samples were taken with a zooplankton net of 45-cm mouth diameter and 333 lm mesh size. A flow meter (Hydro-Bios) was mounted at the centre of the mouth opening. The net was towed obliquely 1 m below the surface. Sampling time was approximately 10 min at the vessel cruise speed of 2 knots. The copepod samples were immediately preserved in a liquid nitrogen container on board ship. Copepods collected at stations 1–3 (ocean outfall area) and station B1 (background station) were analyzed for trace metals.

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Dissolved trace metals (Cd, Co, Cu, Fe, Mn, Ni, Pb, Zn) were extracted using the APDC-DDDC/Freon (ammonium pyrrolidine dithiocarbamate/diethyl diammonium dithiocarbamate) technique modified by Statham (1985). The accuracy of this solvent extraction technique carried out in each analytical batch was assessed by analysing a CASS-3 coastal seawater reference sample (the National Research Council of Canada, NRCC) in triplicate. The ratio of the average result of each group of triplicate analyses to the certified values fell in the range 0.85–1.14. The standard deviation of the triplicate analysis for each metal was normally less than 10% of the average value. The blank values for the analyzed elements were as follows: Cd, 0.04 ± 0.006 nM; Cu, 0.27 ± 0.02 nM; Fe, 2.69 ± 0.18 nM; Mn, 2.46 ± 0.91 nM; Pb, 0.45 ± 0.26 nM; and Zn, 3.15 ± 0.28 nM. Dissolved Cr(VI) was extracted by employing the tricaprylmethyl ammonium chloride (Aliquat-336)/MIBK technique developed by Sirinawin and Westerlund (1997). The MIBK organic solvent was replaced with Freon. The reference sample of dissolved Cr(VI) in seawater is not available in the market. Thus, the recovery of this analytical procedure was assessed by spiking Cr(VI) standard solution in one chosen sample in triplicate. The recovery and analytical blanks of this analytical procedure were 95 ± 8% and 0.21 ± 0.06 nM, respectively. The suspended particulate matter (SPM) loaded filters were rinsed and dried to constant weight in a flow hood at room temperature. The SPM was obtained from the difference in weight of the filter before and after filtration. Each dried loaded filter was soaked in 4 ml of 1 N ultrapure HCl acid (J.T. Baker Ultrex Brand) for 24 h at room temperature. The clear supernatant was separated from the SPM using a centrifuge operated at a speed of 4000 rpm for 5 min and then stored in acid-cleaned polypropylene tubes. Hydrochloric acid was selected because it removes weakly bound or non-detrital trace metals and yields results which correlate well with the biological availability of sedimentary trace metals (Loring & Rantala, 1988, 1992). The standard reference material, MESS-2, supplied by the National Research Council of Canada, was used to establish total particulate metal concentrations. Concentrations of trace metals leached from the MESS-2 reference material indicated that 23.0 ± 2.3% of the certified total Fe, 66.8 ± 5.8% of Co, 23.6 ± 1.3% of Cu, 82.7 ± 4.8% of Mn, 31.1 ± 3.4% of Ni and 31.7 ± 2.3% of Zn was released. The relatively low recovery of Fe, Cu, Ni and Zn, the moderate recovery of Co, and the higher recovery of Mn suggested that our technique removes only the labile fraction of particlebound metals. The detailed analytical procedure is described elsewhere (Fang & Hong, 1999). Trace metals contained in the cleaned Nuclepore polycarbonate filters (n = 3) were as follows: Cd, 0.004 ± 0.001 lg g 1; Co, 0.13 ± 0.01 lg g 1; Cr, 0.15 ± 0.02 lg g 1; Cu, 0.03 ± 0.02 lg g 1; Fe, 0.25 ± 0.10 lg g 1; Mn, 0.02 ± 0.01 lg g 1; Ni, 0.04 ± 0.01 lg g 1; Pb, 0.011 ± 0.003 lg g 1; and Zn, 0.13 ± 0.01 lg g 1. In order to make comparisons between the ocean outfall area and the background stations, three species of dominant copepods were analyzed for trace metals: Temora turbinata, Oncaea venusta and Euchaeta rimana. Both female and male copepods were selected. The abundances of copepods at stations 1, 2, 3 (outfall station) and station B1 (background station) were 1518 inds m 3, 456 inds m 3, 160 inds m 3 and 204 inds m 3, respectively. These numbers were distributed among 14, 8, 16 and 31 different species, respectively. The copepod Temora turbinata accounted for 67–91% and 46% of the total number of copepods at the outfall and background stations, respectively. The number of males was nearly the same as that of females at each station. Temora turbinata and Oncaea venusta are the dominant species of copepods in northern Taiwan (Hsieh & Chiu,

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1998; Hsieh & Chiu, 2002; Hwang et al., 1998; Lo et al., 2004). Another species, Euchaeta rimana, is carnivorous. We selected these species of copepods in our study of the bioconcentration of trace metals in the ocean outfall area. About 100 individuals of each species of copepod were selected and were washed with Milli-Q water three times to remove suspended particulate material prior to analysis. The copepods were then filtered out on an acid-cleaned Nuclepore membrane (0.45 lm) which had been weighed prior to use. The copepod-loaded filters were dried in a laminar flow hood inside a clean room for 48 h. The weight of each copepod sample was obtained as the difference in the weight of the Nuclepore membrane with and without copepod samples. These samples were then digested with 3 ml HNO3 (65%, J.T. Baker Ultrex) for 4 h at 80 C in a Teflon beaker. Digested solutions were made up to 2-ml volumes using sub-boiled distilled water. Trace metals, except for Al, in the above extracted/digested solutions were measured by furnace atomic absorption spectrophotometry (GFAAS) using a Perkin–Elmer Analyst 800. Aluminum was determined with the Lumogallion method of Hydes and Liss (1976) using a Perkin–Elmer LS-50B luminescence spectrophotometer. When metal concentrations in the extracts exceeded that of the highest calibration standard used, the solution was diluted to the proper concentration using 4% ultrapure HNO3 acid and 1 N ultrapure HCl acid for dissolved and particulate metal measurements, respectively. 3. Results 3.1. Dissolved and particulate trace metals Water, particle and copepod samples were analyzed for 10 elements. However, the concentrations of Co and Ni in the copepod samples were below the detection limits for GFAAS. Results for the remaining eight elements, namely, Al, Cd, Cr, Fe, Mn, Pb, and Zn, are discussed in this paper. The concentration ranges of dissolved and leachable particulate metals found in the ocean outfall area were as follows: Cd, 0.03–0.14 nM, 0.03–0.79 lg g 1; Cr, 4.35– 6.86 nM, 4.8–16.4 lg g 1; Cu, 0.36–1.74 nM, 13.4–42.8 lg g 1; Fe, 24.3–92.98 nM, 0.27– 1.36%; Mn, 8.5–24.2 nM, 320–667 lg g 1; Pb, 0.09–0.43 nM, 10.2–24.6 lg g 1; Zn, 10.33–74.89 nM, 18.1–88.6 lg g 1; Al, 66.9–131.39 nM, 0.54–0.85%. Surface concentration contours of dissolved and particulate metals are shown in Figs. 2 and 3. The contours were generated using the Generic Mapping Tools software and interpolation within 100 m · 100 m grids. The sampling depths of middle and bottom layers at each of the stations were not consistent because of the topographical variations. Thus, the concentration contours of trace metals in both phases at the middle and bottom layers in the study area were not available and were unable to judge whether the contours existed any systematic differences among the three layers. 3.2. Trace metals in copepods Concentration ranges of trace metals in copepods were as follows: Cd, 0.23– 1.81 lg g 1; Cr, 16.5–195 lg g 1; Cu, 14–160 lg g 1; Fe, 256–7255 lg g 1; Mn, 5.5– 80.8 lg g 1; Pb, 2.6–56.2 lg g 1; Zn, 132–3891 lg g 1; Al, 0.21–1.13%. Concentrations of trace metals within individual species are shown in Fig. 4. Differences among species

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Fig. 2. Contour plots of dissolved metal concentrations in surface waters of the ocean outfall area.

Fig. 3. Contour plots of particulate metal concentrations in surface waters of the ocean outfall area.

were quite considerable (up to 10–30-fold variations). Aluminum, and probably Fe, was the most abundant trace elements in copepods, while Cd was the least abundant. It can be seen in Fig. 4 that the concentrations of trace metals in copepods collected at the ocean outfall stations were generally higher than those obtained at the background station. The concentrations of trace metals in copepods also varied with different species of copepods.

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The concentrations of Fe, Mn, Pb, and Cu in Temora turbinata, especially among female individuals, were evidently higher than those of the other species at the outfall stations. Such elevated concentrations were not observed for Cd and Cr. Concentrations of Fe, Cr, and Pb in the copepods collected at the background station differed among the different species of copepods, but no such inter-species differences were observed for the other metals.

Fig. 4. Trace metals concentrations in copepods collected at stations 1–3 and at the background station. M, male; F, female.

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4. Discussion 4.1. Dissolved and particulate trace metals Concentrations of dissolved trace metals in marine environments can vary by three orders of magnitude from pristine to heavily polluted environments (Kennish, 1999). Compared with those reported for other trace metal impacted marine environments around the world, such as the San Francisco Bay (Flegal, Smith, Gill, Sanudo-Wilhelmy, & Anderson, 1991) and the Hudson (Klinkhammer & Bender, 1981), Humber (Comber, Gunn, & Whalley, 1995), Seine (Chiffoleau, Cossa, Auger, & Truquet, 1994) and Scheldt (Baeyens et al., 1998) estuaries, dissolved concentrations of Cd, Cu, Fe, Mn, Pb, and Zn found in the present study were generally lower, as shown in Table 1. The published database for dissolved Cr in marine environments is much scantier than that for any of the other metals, partly because the analytical procedure for dissolved Cr in seawater is different from established procedures used for other trace metals (Cranston, 1983; Sirinawin & Westerlund, 1997). It is known that dissolved Cr can exist in two different oxidation states, Cr(III) and Cr(VI), in seawater (Elderfield, 1970). It has been reported that Cr(VI) makes up the largest fraction of total Cr in oxygenated seawater; percentage values range from 75% to 93% (Achterberg & van den Berg, 1997) to more than 95% (Cranston, 1983). The concentration of dissolved Cr(VI) in less polluted coastal or oceanic seawater is generally less than 5 nM (Achterberg & van den Berg, 1997; Sirinawin, Turner, & Westerlund, 2000; and references cited therein). However, relatively high concentrations of total dissolved Cr, 3.5–47 nM (mean value, 17 nM), have been reported for the Abu Kir Bay, east of Alexandria, Egypt (Dahab, 1989). The values of dissolved Cr(VI) found here ranged from 4.4 to 6.9 nM, indicating that the waters in the outfall area were probably not significantly contaminated by Cr. Table 1 Comparison of the dissolved concentrations of trace metals (nM) in the ocean outfall seawater off the Tanshui coast and in other heavily polluted marine environments around the world Location a

Tanshui coast The San Francisco Bayb The Hudson estuaryc The Euripos Straits, Greeced The Humber estuarye The Seine estuaryf The Scheldt estuaryg Port Jackson estuary, Australiah

Al

Cd

Cr(VI)

Cu

Fe

Mn

Pb

Zn

66.9–131.4 ND ND ND

0.03–0.14 ND ND 0.36–3.38

4.35–6.86 ND ND ND

0.37–1.74 9–73 15–97 7.1–325

24.3–93.0 8–1680 15–720 ND

8.5–24.2 ND 8–1100 6.2–56

0.09–0.43 ND ND 0.7–13

10.3–74.9 3.6–28 45–460 39–1835

ND ND ND ND

ND ND 0.09–1.42 0.05–0.89

ND ND ND ND

31–157 26–40 6.3–25.2 14.7–40

ND ND ND ND

6.2–56.1 20–450 ND 6–1838

ND ND 0.14–1.45 ND

54–306 90–200 7.7–191 50–148

ND: no data. a This study. b Flegal et al. (1991). c Klinkhammer and Bender (1981). d Dassenakis et al. (1996). e Comber et al. (1995). f Chiffoleau et al. (1994). g Baeyens et al. (1998). h Hatje et al. (2003).

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In spite of the above findings, it would be worth establishing the current state of contamination by dissolved trace metals in the ocean outfall area off the Tanshui coast. The best approach would unquestionably be to compare concentrations of trace metals in seawater before and after the commissioning of the ocean outfall. Unfortunately, data before ocean outfall commission are not available. In order to overcome this problem, the normalization method can be used to assess the contamination status of trace metals in the study area. Normalization to the background levels of metals in samples with different characteristics can be accomplished by calculating an enrichment factor (EF) relative to the earthÕs crust. In the equation EF = (Mx /Alx )/(Mr /Alr ), Mx and Alx are the metal and aluminum concentrations in the sample, and Mr and Alr are the metal and aluminum concentrations in the crust, respectively (Loring & Rantala, 1992; Luoma, 1990). We have used this criterion to evaluate the contamination status of dissolved and particulate trace metals in the study area. The metal and aluminum concentrations in the crust were replaced with the average concentrations of metal and Al in the all samples taken at the two background stations. The concentration ranges of dissolved and particulate trace metals found at the two background stations are listed in Table 2. Fig. 5 shows enrichment factors of trace metals in dissolved and particulate phases in water samples from the three layers of each station near the outfall. The EF of dissolved iron ranged from 1.32 to 7.51, with an overall mean of 2.86, which was the highest value among the dissolved metals. Thus iron showed the highest enrichment factor of all metals in the dissolved phase. Zinc ranked second with an average value of 1.56. Although some values of the EF of Cd, Cr(VI), Cu, Mn, and Pb were greater than 1, the average value of the EF of these elements was generally less than 1, so that no contamination can be demonstrated for these elements in seawater near the outfall. The SPM in inshore environments originates from multiple sources. Thus, the concentrations of chemical constituents in SPM in different marine environments can vary one to two orders of magnitude (e.g., Turner, Millward, & Morris, 1991). Trace constituents in the SPM can be associated with a variety of sedimentary components, which can enter into biogeochemical reactions to different extents. Analysis of the total content of trace metals in the SPM includes material which is located in the lattice structure of minerals and is unavailable for such reactions under most environmental conditions. Tessier, Campbell, and Bisson (1979) pioneered the development of sequential extraction procedures for separating different forms of trace metals in particles/sediments. Their original analytical procedure is somewhat time-consuming and tedious. Some researchers prefer to employ a one-step extraction procedure, using either weak or diluted strong acids, to determine the particulate metals in ligand-exchangeable, carbonate-bound, Fe and Mn oxide-bound and organic forms (Loring & Rantala, 1988, 1992; and references cited therein). This one-step extraction procedure is easy to apply and is considered a useful tool for differentiating anthropogenic from background levels of different contaminants (Loring & Rantala, 1988, 1992). However, Martin, Nirel, and Thomas (1987) pointed out that there are some disadvantages to this approach: (1) re-adsorption can occur at neutral pH; (2) the use of a single reagent does not permit the dissolution of all the organic and inorganic labile forms without also removing part of the inert, detrital fraction. Strictly speaking, it is not appropriate to directly compare the concentrations of particulate trace metals obtained from different inshore environments and analyzed with different

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Dissolved trace metals (nM) Al Cd 56.7–86.5 (71.0) 0.077–0.109 (0.097)

Cr(VI) 4.13–4.64 (4.42)

Cu 0.59–0.68 (0.63)

Fe 12.3–13.9 (13.1)

Mn 11.0–12.2 (11.7)

Pb 0.14–0.17 (0.16)

Zn 13.8–17.5 (15.8)

Particulate trace metals SPM (mg L 1) Al (%)

Cd (lg g 1)

Cr (lg g 1)

Cu (lg g 1)

Fe (%)

Mn (lg g 1)

Pb (lg g 1)

Zn (lg g 1)

6.29–7.95 (7.36)

0.36–0.54 (0.43)

5.93–6.61 (6.28)

14.45–18.16 (15.95)

0.67–0.88 (0.75)

310–337 (323)

6.31–8.38 (7.19)

8.68–9.26 (8.96)

0.43–0.57 (0.50)

Number in parentheses: mean value.

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Table 2 The concentration ranges of dissolved and particulate trace metals, and of suspended particulate matter (SPM) in all samples taken at two background stations

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Dis. trace metal Par. trace metal

1

Cu enrichment factor

Cr enrichment factor

Cd enrichment factor

4

3

2

2

1

0 1 2 3 4 5 6 7 8 9 10 11 12 13

2 1 0

0

0

3

0 1 2 3 4 5 6 7 8 9 10 11 12 13

0 1 2 3 4 5 6 7 8 9 10 11 12 13

3

5

4 3 2 1

Pb enrichment factor

Mn enrichment factor

Fe enrichment factor

5

2

1

0 1 2 3 4 5 6 7 8 9 10 11 12 13

0 1 2 3 4 5 6 7 8 9 10 11 12 13

3 2 1 0

0

0

4

Station

Station

0 1 2 3 4 5 6 7 8 9 10 11 12 13

Station

Zn enrichment factor

10 8 6 4 2 0 0 1 2 3 4 5 6 7 8 9 10 11 12 13

Station

Fig. 5. Enrichment factors for dissolved and particulate metals in all samples collected at the ocean outfall stations.

analytical procedures. On the other hand, a comparison with other marine environments affected by effluents from ocean outfalls could be informative. Table 3 lists the concentrations of trace metals in particles or sediments in some ocean outfall environments that are adjacent to the metropolitan areas. The concentration ranges of particulate metals found in this study are on the same order of magnitude as those of the other ocean outfall environments. In contrast to the result for dissolved metals, the average value of the EF of particulate Cr, Cu, Pb, and Zn was greater than 1, and that of particulate zinc, with an average of 4.5, was the highest (Fig. 5). The average value of the EF of particulate Fe and Mn approached

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Location

Particles/sediment

Analytical method

Al

Cd

Cr

Cu

Fe

Mn

Pb

Zn

Tanshui coasta Sydney continental shelfb Santa Monica Bayc Vancouver Islandd Arabian Gulfe Havana Bayf

Particles

1 N HCl 24 h

0.54–0.85

0.03–1.11

4.75–16.39

13.39–70.8

0.27–1.36

320–667

10.23–35.8

18–116

Particles

HNO3/HCl (USEPA method 3050A)

ND

ND

35–168

15–1360

1.4–4.6

63–684

22–285

94–2307

Sediment

ND

0.3–4.9

35–110

0–70

ND

ND

6–37

46–128

ND

<0.1–0.7

31.8–59.4

16.6–197

ND

ND

8.2–129

7.7–197.7

Sediment

HNO3/HCl (USEPA method 3050A) HNO3/HCl (USEPA method 3050A) Conc. HNO3 120 C 3 h

ND

0.73–31.6

2.69–23.2

0.01–32.2

0.07–11.8

11.7–196

4.7–46.3

2.1–33.6

Sediment

0.5 N HCl

ND

ND

49–124

14–1075

0.3–7.77

68–279

321–768

294–980

Sediment

The metal concentration unit is lg g ND: no data. a This study. b Matthai et al. (2002). c Bay et al. (2003). d Chapman et al. (1996). e Sadiq (2002). f Gonzalez et al. (1999).

1

except for Al and Fe in percentage.

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Table 3 Comparison of the concentrations of trace metals in particles or sediments in various ocean outfall environments around the world

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1, indicating that the concentrations of both particulate metals in the ocean outfall area paralleled the values at the background stations. The value of the EF of particulate Cd ranged from 0.04 to 1.75, with an average of 0.35, suggesting that Cd had the least impact among the particulate metals. It is known that most trace metals have high affinity for suspended particulate matter in marine environments (Balls, 1989). As a result, it is often found that trace metal partitioning in seawater is heavily weighed towards the particulate phase, especially so in regions of anthropogenic influence (Fang & Lin, 2002; Matthai et al., 2002; Turner et al., 1991). Particulate metals eventually settle to the bottom and may be directly available to benthic fauna (Langston, 1990) or may be released to the water column through sediment resuspension, adsorption/desorption reactions, reduction/oxidation reactions, or the degradation of organisms (Santschi, Hohener, Benoit, & Brink, 1990). These processes could enhance the dissolved concentrations of trace metals in the environment and threaten the ecosystem. In addition, many studies have indicated that the transport, accumulation, and fate of particle-reactive trace metals in coastal environments are governed to a significant extent by a combination of particle transport dynamics and chemical phase transfer processes (Balls, 1989; Fang & Lin, 2002; Millward & Turner, 1995). Thus, to better understand the geochemical fate of trace metals, it is necessary to know the partitioning between dissolved and particulate trace metals in the ocean outfall area. The trace metals measured here can be divided into four groups according to their fractionation profiles: (1) Al, Cu, Mn, and Pb; (2) Fe; (3) Zn and Cr; (4) Cd. The average percentages of these metals associated with SPM were as follows: >85%, 70%, 15–30%, and <5%, respectively. They followed the sequence: Al(95%) = Mn(95%) > Pb(88%) > Cu(86%) > Fe(72%) > Zn(32%) > Cr(17.5%) > Cd(3.4%). With the exception of Cu, this sequence is generally in agreement with those found in other marine environments (Balls, 1989; Dassenakis, Kloukiniotou, & Pavlidou, 1996; Muller, Tranter, & Balls, 1994; Wells, Smith, & Bruland, 2000). However, the percentage of particulate-bound Cu found in the present study was significantly higher than those reported in the above studies (<40%) in which it is argued that the stability of Cu–organic complexes in solution tends to reduce its adsorption onto particulate matter (Muller et al., 1994; Wells et al., 2000). The reason why Cu dominated in particulate phase in this study is not clear and needs further investigation. This result may also explain why the values of the enrichment factors of Cu, Pb, and Zn in particulate phase were greater than those of these elements in dissolved phase. In addition, the enrichment factor of particulate Cd had the smallest value among the metals studied. The result of the partitioning of Cd in the present study agreed well those of many studies, which showed that more than 95% of the Cd was present in the dissolved phase, as Cd can be stabilized in solution through the formation of stable chloro-complexes (Bourg, 1987). 4.2. Trace metals in copepods Few concentrations of trace metals in marine copepods have been reported in the literature. Ritterhoff and Zauke (1997), who determined the trace metals contained in zooplankton from the Fram Strait and the Greenland Sea, found that the concentrations of trace metals in copepods were in the following ranges Cd, 0.1–0.7 lg g 1; Cu, 3.8– 7.5 lg g 1; Pb, <0.5 lg g 1; and Zn, 86–389 lg g 1. Ritterhoff and Zauke (1997) also reported the following bioconcentration factors of copepods for trace metals: Cd, 5.2;

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Cu, 4.9; Pb, 3.9; Zn, 5.9. The corresponding concentrations for Pb and Zn, but with relatively higher concentrations of Cd (2.3–14.4 lg g 1) and Cu (6–52 lg g 1), were reported for various Antarctic copepods, such as Rhincalanus gigas, Calanus propinquus, Calanoides acutus, Metridia curticauda and Metridia gerlachei (Kahle & Zauke, 2003). The concentrations of Cu, Pb, and Zn in copepods in the present study were somewhat higher than those found in the Fram Strait, the Greenland Sea, and the Antarctic. In addition, the accumulation factor of both Cu and Pb was one to two orders of magnitude higher than that found in the Fram Strait and the Greenland Sea. The reason for these results probably lies in the fact that the environment of the present study area was more contaminated by trace metals than the pristine environments found in the Greenland Sea and the Antarctic. On the other hand, inter-species differences in the metal quota of copepods also need to be taken into consideration, as shown in Fig. 4. Excess metals in seawater results in high concentrations of metals in biota through bioconcentration. Bioconcentration the process by which a chemical species is accumulated into biota from its surrounding environment but at a higher concentration. The bioconcentration factor (BCF) can provide general information about how enriched in particular elements organisms are with respect to its surrounding environment. Based on the copepods and water samples data from the surface layer of water column, mean values of the BCF (Cm/Cw, Cm and Cw represent the metal concentration in copepods and water, respectively) of marine copepods for trace metals in the present study generally fell in the range of 4–7 and followed the sequence: Al(6.4) > Cu(6.2) > Fe(6.0) > Zn(5.7) > Pb(5.6) > Cr(5.5) > Cd(5.1) > Mn(4.7). The elemental BCF sequence presented above agrees well with previously published data for copepods and amphipods (Kahle & Zauke, 2002, 2003). For a given element, the BCF of different species of copepods varied within less than 1–2 orders of magnitude, as shown in Fig. 6. Surprisingly, the average value of Mn BCF of copepods was the smallest among 8

Log (bioconcentration factor)

7 6 5 4 3 2 1 0

Al

Cd

Cr

Cu Fe Element

Mn

Pb

Zn

Fig. 6. Trace metal bioconcentration factors in copepods obtained in this study.

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the elements studied. There are very few published values of Mn concentrations in marine copepods (Ritterhoff & Zauke, 1997; Kahle & Zauke, 2002, 2003; Wang & Fisher, 1998). It was reported that the Mn concentrations in three species of talitrid amphipods in the Gulf of Gdansk region were in the range 13–109 lg g 1 (Fialkowski, Rainbow, Smith, & Zmudzinski, 2003), and these values are in good agreement with those of the copepods studied here. The dissolved concentration of Mn in inshore environments generally ranges from 10 to 500 nM (Table 1). Thus, the bioconcentration factor, calculating from the average concentration of Mn in organisms, such as the copepods or amphipods, and in seawater, approaches a value of 5, which is confirmed by our findings. Differences in bioconcentration factors can be attributed to two factors: the concentration factor in the algal food (that is, the degree of metal enrichment in algae) and the assimilation efficiency of the metals in the copepods (Hook & Fisher, 2002). The concentration factor for Mn in diverse marine phytoplankton has been estimated at 6 · 104 (IAEA, 1985). Hook and Fisher (2002) showed that concentration factors in diatom cells were 1.8 · 104 for Cd, 1.9 · 105 for Zn, and 8.5 · 103 for Mn, and that the assimilation efficiencies of trace metals by Acartia tonsa and Acartia hudsonica were 62% for Cd, 55% for Zn and 15–30% for Mn. This result may also explain why the BCF of Cd and Mn in marine copepods is relatively small, as found in the present study. Many studies have shown that chemical pollutants may affect copepods to various degrees ranging from sub-lethal to lethal effects, and thus impact copepods population dynamics (Hook & Fisher, 2001a, 2001b; Lindley, George, Wvans, & Donkin, 1998; Saunders & Moore, 2004; Stalder & Marcus, 1997). Hook and Fisher (2001a, 2001b) investigated the effect of exposure route on metal accumulation, tissue distribution, and toxicity in the marine copepods A. hudsonica and A. tonsa. Their results show that metals taken up through food can depress egg production in marine copepods when phytoplankton prey were exposed to 1 nM Hg or 5 nM Cd. They also indicate that this effect occurs when the metal burden in copepods increases only a few-fold over background levels. They further suggest that metals interfere with egg production by altering vitellogenesis so as to decrease yolk accumulation in the developing ovary. Similar results have also been reported by Lindley et al. (1998) who examined the viability of copepod resting eggs from British estuaries in which the degree of chemical contamination varied. Their results demonstrate that the highest hatching success (92%) was observed for resting eggs from the estuary having the lowest concentration of PAHs. Conversely, lowest hatching success (14%) occurred in the estuary with the highest concentration of PAHs. A recent study conducted by Saunders and Moore (2004) investigated the influence of copper pollution on benthic copepod by dosing seabed sediments with copper. It also revealed that copepod abundance was significantly depressed in the high-copper (nominal 5000 lg g 1) treatment. This study examined, for the first time, trace metal levels in the copepods found in the marine environment off northern Taiwan. Copepods collected at the ocean outfall stations had relatively higher concentrations of trace metals. Copepods collected at the background station exhibited greater species diversity but lower abundance than those at the outfall stations. There are two possible explanations for this result. One is that the seawater at the background station was influenced by the Kuroshio Branch Current intrusion. The other is that the effluents from the ocean outfall encouraged the growth of a more limited range of copepods species. It has been shown that fisheries in the Japanese Seto Sea benefited dramatically from the increase in organic discharges (Clark, 2001). This phenomenon cannot

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be excluded to explain the result found in this study. An understanding of the full ecological impact of ocean outfall discharges in northern Taiwan will only be obtained through longer-term monitoring. 5. Conclusion This study investigated trace metals in seawater and copepods in the ocean outfall area off the northern Taiwan coast. Relative enrichment factors of dissolved Fe and Zn, and of particulate Cr, Cu, Pb, and Zn were found to be greater than 1, implying that the waters around the ocean outfall area were contaminated by these metals to some degree. In addition, the particulate phase contributed more than 70% of total Al, Cu, Mn, Pb and Fe concentrations in seawater. In contrast, the dissolved phase contributed more than 70% of the total Zn, Cr, and Cd. A reasonably good correlation was found between metal contamination in seawater around the ocean outfall area and concentrations in the tissues of copepods. The concentrations of trace metals in copepods collected in the ocean outfall area were generally higher than those obtained at the background station, and this observation held particularly strongly for Temora turbinata. Bioconcentration factors of copepods ranged from 4 to 7, suggesting that copepods have a great capacity to accumulate trace metals, and thus can serve as biological indicators to assess metal contamination and impact in the marine environment. Acknowledgements This research was financially supported by Sinotech Engineering Consultants Ltd. and by the National Science Council of the Republic of China under NSC Grants 90-2611-M019-007 and 91-2611-M-019-005. The authors are grateful to two anonymous referees for their constructive comments and suggestions which led to significant improvements to the manuscript. Dr. F.L. Muller at University of Bergen, Norway, is thanked for helping to make the English more readable. The authors are also grateful to C.F. Chen and C.H. Wang for the sampling and sample analysis. References Achterberg, E. P., & van den Berg, C. M. G. (1997). Chemical speciation of chromium and nickel in the western Mediterranean. Deep Sea Research II, 44, 693–720. Baeyens, W., Parmentier, K., Goeyens, L., Ducastel, G., De Gieter, M., & Leemarkers, M. (1998). The biogeochemical behavior of Cd, Cu, Pb and Zn in the Scheldt estuary: results of the 1995 surveys. In W. F. J. Baeyens (Ed.), Trace metals in the Westerscheldt estuary: a case-study of polluted, partially anoxic estuary (pp. 45–62). Dordrecht/Boston/London: Kluwer Academic Publishers. Balls, P. W. (1989). The partition of trace metals between dissolved and particulate phases in European coastal waters: a compilation of field data and comparison with laboratory studies. Netherlands Journal of Sea Research, 23, 7–14. Barka, S., Pavillon, J. F., & Amiard, J. C. (2001). Influence of different essential and non-essential metals on MTLP levels in the copepod Tigriopus brevicornis. Comparative Biochemistry and Physiology Part C, 128, 479–493. Bay, S. M., Zeng, E. Y., Lorenson, T. D., Tran, K., & Alexander, C. (2003). Temporal and spatial distributions of contaminants in sediments of Santa Monica Bay, California. Marine Environmental Research, 56, 255–276. Bothner, M. H., Casso, M. A., Rendigs, R. R., & Lamothe, P. J. (2002). The effect of the new Massachustts Bay sewage outfall on the concentrations of metals and bacterial spores in nearby bottom and suspended sediments. Marine Pollution Bulletin, 44, 1063–1070.

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