Research Dynamic Model for the Accumulation of Cadmium and Zinc from Water and Sediment by the Aquatic Oligochaete, Tubifex tubifex ERIK STEEN REDEKER,* LIEVEN BERVOETS, AND RONNY BLUST Ecophysiology, Biochemistry and Toxicology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium
In aquatic environments, organisms are exposed to and accumulate metals via waterborne and dietary routes including ingested sediment. A key element in understanding metal uptake and accumulation is information concerning the relative importance of the routes of uptake and the kinetics of the processes. In this work the bioaccumulation of the essential element zinc and the nonessential element cadmium were studied from the aqueous and sediment phase, in the cosmopolitan oligochaete Tubifex tubifex, using the radiotracers 109Cd and 65Zn. A compartmental kinetic model was constructed and parametrized by fitting the model to metal body concentrations. Using the pharmacokinetic modeling approach and taking into account the distribution of the metal between water and sediment, the different routes were quantitatively separated. Under the experimental conditions, the sediment phase accounted for 9.8% of the cadmium and 52% of the zinc uptake. These values are based on the uptake of the radiotracers spiked sediments and therefore likely represent maximal values since it was shown that under the specific conditions this was the most mobile metal fraction. This difference was largely explained by the large difference in assimilation efficiency between cadmium and zinc. Simulations of different conditions showed that both dissolved and sediment-associated metal can be important sources of metal exposure for the worms and that the relative importance strongly depends on the metal and exposure conditions including the lability of the metals in the sediment phase.
Introduction The pollution of aquatic ecosystems with metals is a serious threat to the environment due their persistent nature, long distance transport, and toxicity to aquatic organisms (1). Heavy metal pollution in aquatic ecosystems is usually monitored by chemical measurements of concentrations in water or sediment. Although measurements of total metal concentrations provide useful information on the pollution status of the environment, they do not provide a direct * Corresponding author phone: +32 (0)3 265 33 44; fax: +32 (0)3 265 34 97; e-mail:
[email protected]. 10.1021/es0496470 CCC: $27.50 Published on Web 11/29/2004
2004 American Chemical Society
indication of the bioavailability, bioaccumulation, or toxicity of metals to aquatic organisms (2). In aquatic ecosystems, sediments serve as both a sink and a source of pollutants (3). The sediments often contain a complex mixture of contaminants at concentrations that can be orders of magnitude higher than in the overlying water (4). For the assessment of the risks associated with contaminated water and sediments, it is important to determine the importance of these different routes of exposure for metal uptake, accumulation, and toxicity. In the aquatic environment metals are present in different forms or species and distributed among solute, colloidal and particulate phases (5). Benthic organisms, living at the interface between water and sediment, can take up and accumulate metals from both aqueous and solid sources (6). The benthic fauna is of great importance because it represents an essential link in the aquatic food web and can therefore pose a threat for possible transfer to higher trophic levels (7). One of the most widespread benthic groups, ubiquitous in aquatic habitats, are the tubificid oligochaetes (8). The cosmopolitan aquatic oligochaete, Tubifex tubifex (Mu ¨ ller, 1774) is one of the oldest described aquatic oligochaetes (9) and can be found in both nonpolluted and very polluted areas (10). The species has a reputation for being very resistant, though not insensitive to pollution, and is often one of the last to disappear from a contaminated site (11, 12). In addition, it can adapt to a wide range of environmental conditions (10) and has therefore been used as a bioindicator of environmental pollution (12). Despite the importance of oligochaetes for the functioning of aquatic ecosystems and the fact that T. tubifex has been used as a test organism to assess the toxicity of various metals in water (6, 7, 11, 13, 14) and sediments (8, 10, 15, 16), little is known concerning the importance of different exposure routes on metal uptake and accumulation. Since benthic invertebrates can take up and accumulate metals from different sources, the determination of the relative importance of the routes of uptake is indispensable to relate metal uptake to accumulation and toxicity for these or other organisms. The aim of the present work is to determine the importance of the aqueous and sediment phase as exposure sources of a nonessential (cadmium) and an essential metal (zinc) for the oligochaete worm, T. tubifex. The organisms were exposed to cadmium and zinc through either the aqueous or sediment phase. The uptake, accumulation, and elimination of cadmium and zinc were followed using radiotracers. The results of the uptake and elimination experiments were fitted to a multicompartmental pharmacokinetic model. The pharmacokinetic parameters derived by the model were used to quantitatively separate both exposure routes. Additionally, the influence of different exposure scenarios such as metal partitioning on the relative contribution of the exposure phases in the bioaccumulation of cadmium and zinc are discussed.
Materials and Methods Test Species and Exposure Solutions. Test organisms were collected from the Scheldt River near Kruibeke, Belgium, from the upper layer of the sediment at low tide. The organisms were transported to the lab in their natural sediment. Upon arrival, the sediments were sieved over a 1 mm sieve. The tubificidae were selected for equal size and carefully transferred to aquaria with reconstituted freshwater VOL. 38, NO. 23, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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(medium hard freshwater (OECD, 1993) containing CaCl2, 2.0 mM; MgSO4, 0.5 mM; NaHCO3, 770 µM; KCl, 77 µM; pH 7.7, hardness 250 expressed as mg/L CaCO3 (17)). The organisms were allowed to acclimatize in reconstituted freshwater for 7 d prior to the experiments. The water in the aquaria was kept at 15 ( 0.5 °C and constantly aerated. The worms were fed a suspension of finely grounded TetraMin flakes (Tetra Werke, Germany), and the water was changed daily. The feeding of the organisms was stopped 48 h before the start of the experiments. The experiments were conducted at 15 ( 0.5 °C under a natural light/dark regime. For the experiments, the organisms were randomly placed in the exposure solutions or sediments. During the experiments, the animals were not fed and the water was not aerated. Cd and Zn were added from a stock solution as CdCl2 (CdCl2 monohydrate, Merck, extra pure) or ZnCl2 (Merck, pro analyze) in reconstituted freshwater. Accumulation from the Aqueous Phase. The accumulation and elimination characteristics of cadmium and zinc from the aqueous phase by T. tubifex were determined using a radiotracer technique. The organisms were exposed to a metal containing solution spiked with the corresponding radioactive tracer. The spiking solutions were made by adding 200 kBq/L radioactive 109Cd and 65Zn to a solution of 0.1 µM cadmium and 1 µM zinc (specific activity 2000 and 200 kBq µmol-1, respectively). For each individual experiment, 10 organisms were exposed to 50 mL of the spiked cadmium and zinc solution in 100-mL polypropylene beakers. Periodically, the organisms were removed from the exposure solution and rinsed with reconstituted freshwater, and the radioactivity was measured by γ counting (Minaxi auto-gamma 5000 series, Packard) for 5 min. After γ counting, the organisms were placed back in the exposure solution. After approximately 4 d of exposure, the worms were transferred to solutions without the addition of the radiotracers to follow the elimination of the tracers for another 8 d. Periodically, the organisms were removed from the solution, counted for their radioactivity for 5 min, and placed back in the solution. The experiments were performed in three replicates. The pH and O2 remained constant during the experimental period (pH, 7.70 ( 0.2; O2, 9.6 mg/L ( 0.4). Accumulation from the Sediment Phase. Sediments were collected from the Scheldt River, near Kruibeke (Belgium), at low tide. The 1 cm top layer of the sediments was taken and transported to the lab in airtight containers. The sediments were immediately sieved (
