Environ. Sci. Technol. 2002, 36, 40-47
Metal Exposure and Bioavailability to a Marine Deposit-Feeding Sipuncula, Sipunculus nudus QI-LUN YAN AND WEN-XIONG WANG* Department of Biology, The Hong Kong University of Science and Technology (HKUST), Clear Water Bay, Kowloon, Hong Kong, China
Sediments often constitute the major repository of metals and may be a potential source for metal bioaccumulation by marine deposit- and suspension-feeding invertebrates. In this study, we compared the uptake of Cd, Cr, and Zn from solute and sedimentary sources by a depositfeeding peanut worm, Sipuncula nudus. The uptake rate constants determined for the three metals were generally low and were 0.0016-0.0020 l g-1 d-1 for Cd, 0.01070.0269 l g-1 d-1 for Cr, and 0.0235-0.0463 l g-1 d-1 for Zn. The uptake rate of Zn increased at a disproportionately slower rate with increasing Zn concentrations in the ambient water, indicating that Zn may have been partially regulated at a high Zn concentration. The assimilation efficiency (AE) of the metals was determined using a pulse-chase radiotracer technique. The AEs were in the range of 6-30% for Cd, 0.5-8% for Cr, and 5-15% for Zn. The sediment grain size and radiolabeling duration (between 7 and 30 d) did not affect the metal AE. There was no major difference in the metal AE from natural sediment collected from a contaminated environment. The desorption of metals from the radiolabeled sediments was also concurrently measured using the gut juice extracted from the sipuncula. Up to 63% of Cd was extracted by the gut juice, whereas only 98% of Cd, Co, Se, and Zn in a polychaete Neresis succinea was derived from sediment ingestion, largely as a result of the high feeding rate of the animals and the high partition coefficient of metals in sediment. The relative importance of sediment vs aqueous uptake (either from overlying water or porewater) is highly specific for different groups of organisms. In a more recent study, Hare et al. (22) showed that benthic invertebrates (oligochaete, insects) accumulated the majority of their Cd from the water column as compared with the sediments, likely caused by their burrowing and irrigation behavior. In this study, we examined the bioavailability of Cd, Cr, and Zn to a marine deposit-feeding invertebrate, namely, the sipunculid Sipunculus nudus. The sipuncula (peanut worm) is abundant in the southern China regions and is widespread around the world’s ocean from the Arctic to tropical waters (23). It is in fact an edible marine species and has long been used as a special dish in southern China. The digestive system in this species is in sharp contrast to most other deposit-feeding worms. The mouth and anus are on the same side of the body, with guts typically >1.3-2.3 times of the length of the whole body. We used the AE and gut juice extraction to compare metal bioavailability from sediments in sipuncula. A kinetic model was further employed to quantify the relative importance of sediment as source for metal accumulation in the peanut worms. 10.1021/es015604x CCC: $22.00
2002 American Chemical Society Published on Web 11/28/2001
Materials and Methods The sipuncula (S. nudus) were collected from a mudflat in Ting Kok, Tolo Harbor, Hong Kong. The sizes of the animals were about 5-7 cm, and the tissue dry weights were about 0.3-0.4 g. The animals were maintained in a tank with sediments collected from the same location and running seawater at 23 °C and salinity 29 psu. The experiments were conducted after the animals were acclimated to laboratory conditions for about 1-2 weeks. Cd, Cr, and Zn were examined in this study. These metals were studied using appropriate radiotracers: 109Cd (t1/2 ) 462 d, in 0.1 N HCl), 51Cr(III) (t1/2 ) 27.7 d, in 0.1 N HCl), and 65Zn (t1/2 ) 244 d, in 0.1 N HCl). All isotopes were obtained from New England Nuclear, Boston, MA. Metal Uptake from the Dissolved Phase. Uptake of metals from the dissolved phase by the sipuncula was measured over a 24-h exposure period at different metal concentrations. Metal concentrations in the dissolved phase were 2, 5, 20, and 50 µg L-1 for Cd (as CdCl2) and Cr(III) (as CrCl3) and 5, 20, 50, and 100 µg L-1 for Zn (as ZnCl2). Radioisotope additions were 9.2 kBq L-1 for Cd (corresponding to 0.12 µg L-1), 22.2 kBq L-1 for Cr (2.4 ng L-1), and 18.5 kBq L-1 (1.8 ng L-1) for Zn. Microliter amounts of 0.5 N NaOH were added to maintain the seawater pH due to the addition of the acidic isotopes. The sipuncula were evacuated of their gut contents for at least 1 d before the dissolved uptake experiment. The metals and radioisotopes were equilibrated overnight before the experiments (allowing sufficient ligand exchange). The animals were individually added into 500 mL of 0.22-µm filtered seawater spiked with radioisotopes and metals. There were 5 replicated individuals in each concentration treatment. The water was changed at 8 and 16 h after the initial exposure. At 2, 5, 8, 12, 16, and 24 h, the sipuncula was removed and rinsed with filtered seawater, and the radioactivity was counted. A 2-mL water sample was also taken for radioactivity measurements. Any feces produced during the exposure period were immediately removed. At the end of exposure, the sipuncula were dried at 80 °C for 1 d before the dry weight measurement. Trace Metal Assimilation from Sediments. We measured the assimilation efficiency of metals by the sipuncula feeding on sediments of different sizes, sediments radiolabeled for different durations, and sediments collected from a contaminated site. In sediment grain size experiment, the sediments were collected from a relatively clean site in Hong Kong (Sai Kung) and were wet sieved through different sizes of nylon mesh to generate different particle sizes (40-60, 60-250, 250-500 µm). On the basis of the gut content analysis, the sipuncula was a nonselective deposit-feeder. The sediments (400 mg in 5 mL of 0.22-µm filtered seawater) were spiked with 109Cd, 51Cr, and 65Zn. Radioisotope additions were 37 kBq for 109Cd, 55.5 kBq for 51Cr, and 55.5 kBq for 65Zn. NaOH was added to maintain the normal seawater pH. The sediments were swirled twice a day during the radiolabeling period. After 7 d of radiolabeling, the sediments were centrifuged twice to remove the weakly bound metals. Over 90% of all three radioisotopes were radiolabeled onto the sediment within the 7-d period. In the radiolabeling duration experiment, the sediments (60-250 µm, 0.5-2.0 g in 5 mL) were collected from the clean site in Hong Kong (Sai Kung) and radiolabeled with 109Cd, 51Cr, and 65Zn. Radioisotope additions were 37 kBq for 109Cd, 55.5-111 kBq for 51Cr, and 55.5-74 kBq for 65Zn. NaOH was also added to maintain the normal seawater pH. The sediments were radiolabeled for 7, 15, and 30 d, respectively, before the assimilation experiment, which was conducted simultaneously for different treatments using the same batch of worms, thus the spikes were conducted at different periods of time. In the third experiment, sediments were collected from four stations in a contaminated bay area (Liaolin, China)
TABLE 1. Metal Concentrations (µg g-1) in Natural Sediments Collected from Different Locations in a Contaminated Site (Liaolin Bay, China) and Used in Metal AE Measurementsa site
Cd (µg g-1)
Cr (µg g-1)
Zn (µg g-1)
A B C D clean site
9.0 ( 0.0 6.9 ( 0.1 2.6 ( 0.1 8.0 ( 0.0 74% for Zn) for metal accumulation by the sipuncula even though the AE was as low as 1%. Consequently, sediment should be considered as a direct route for metal accumulation in these ecologically and economically important benthic worms.
Acknowledgments We thank Ms. Wenhong Fan for her help in measuring metal concentrations in sediments. We are very grateful to the anonymous reviewers for their insightful and constructive comments on this work. This study was supported by a
Competitive Earmarked Research Grant from the Hong Kong Research Grant Council (HKUST6113/00M) to W.-X.W.
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Received for review July 11, 2001. Revised manuscript received October 2, 2001. Accepted October 17, 2001. ES015604X
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