Hydrobiologia (2005) 540:169–180 Ó Springer 2005 P. Meire & S. van Damme (eds), Ecological Structures and Functions in the Scheldt Estuary: from Past to Future DOI 10.1007/s10750-004-7134-7
Primary Research Paper
Temporal and spatial trends in heavy metal concentrations in the marine mussel Mytilus edulis from the Western Scheldt estuary (The Netherlands) Valentine K. Mubiana*, Diab Qadah, Joris Meys & Ronny Blust Laboratory of Ecophysiology, Biochemistry & Toxicology Department of Biology, University of Antwerp Groenenborgerlaan 171, B-2020 Antwerp, Belgium (*Author for correspondence: E-mail:
[email protected])
Key words: heavy metals, mussels, Scheldt estuary, salinity and pollution gradient, bioavailability, temporal and seasonal variations
Abstract Since the first North Sea Conference (1984, Bremen), all countries bordering the North Sea made commitments to reduce discharge of hazardous substances into the North Sea. From Belgium and The Netherlands, large reductions (upto 90%) in heavy metal emissions from land-based sources have been reported between 1985 and 2000. Recently, some studies in the Western Scheldt estuary (WS) have shown that total metal concentration in the water, sediments and suspended particles have decreased compared to levels in the 70s. However, data on aquatic organisms is still very limited and it is therefore difficult to confirm whether the reductions in pollution input and generally improving water quality in the WS have a corresponding impact on the levels of heavy metals in aquatic organisms. The current study measured metal concentrations in the soft tissues of mussels, Mytilus edulis (known to be good indicators of environmental metal pollution) during the period 1996–2002. Spatial (salinity and pollution gradients), temporal and seasonal variations were also studied. Results showed a down-stream decreasing trend for the metals studied (Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb and Zn) during all sampling campaigns. There was also a significant seasonal effect on tissue metal concentrations, with a peak observed around spring in both WS and the nearby less polluted Eastern Scheldt (ES). On temporal trends, a clear drop of metals in mussels was observed in the early 80s coinciding with the start of the efforts to reduce chemical pollution input into the North Sea. Since those early reductions, metal concentrations in mussels generally remained unchanged upto mid 90s. However, in recent times metal concentration in mussels have increased significantly, for example Cd in 2002 was almost 10 times the values in 1983 and similar to levels seen during the peak in the 70s. Other metals also increased in the 90s also reaching levels seen in the 70s. As there is no indication of recent increase in metal input into the estuary, we suggest that increased metal concentrations observed in mussels in recent years especially in the upper estuary are most likely a result of changes in physical and chemical speciation and metal bioavailability. Such changes may be caused by changes in some water quality parameters in the estuary (i.e. increased dissolved oxygen, concentration of organic matter), resulting in conditions that favour releases of sediment-bound metals into the water column. The relationship between metal content and season showed very similar annual profiles in the polluted WS and less polluted ES. Thus, seasonal variations in metal concentrations appear to be largely controlled by biological processes, while total body burdens are dependent on environmental levels and bioavailability. Introduction It is well-known that mussels are good indicators of chemical pollution in coastal and estuarine waters.
For a long time, they have been used to monitor metal pollution in coastal and marine environments world-wide (Goldberg, 1983; Luten et al., 1986; Livingstone & Pipe, 1992; Stronkhorst, 1992;
170 De Kock & Kramer, 1994; O’Connor et al., 1994; Widdows et al., 1995; Beliaeff et al., 1997; O’Connor, 1998). In the Dutch coastal and estuarine waters, monitoring of selected heavy metals in marine mussel Mytilus edulis and flounder Platichthys flesus started around 1979 as the Dutch contribution to the Joint Monitoring Programmes (JMP) initiated after the Oslo Convention on dumping at sea (1972) and the Paris Convention on pollution from land-based sources (1974). In later North Sea Conferences, the bordering states agreed on reductions of micropollutant loads into the North Sea and significant reductions have been recorded since 1985. As part of the JMP, Luten et al. (1986) and Stronkhorst (1992) reported concentrations of Hg, As, Cu, Cr, Zn, Pb and Ni in mussels at selected sites in the Western Scheldt estuary (WS) and the nearby Eastern Scheldt tidal basin (ES) for the periods 1979–1983 and 1985–1990, respectively. More recent data is compiled annually by The Netherlands Institute for Fisheries Research – RIVO (Yerseke, The Netherlands). However, under the JMP only a limited number of sites are monitored regularly mostly in the lower estuary. Therefore, long-term temporal profiles are only available for one site Vlissingen (Sal 29 ppt), though one more site in the upper estuary was also included in the 1979–1983 sampling (Luten et al., 1986). In the current study, recent data (1999– 2002) covering all sectors of the estuary are presented. The studies of Luten et al. (1986) and Stronkhorst (1992), both showed no clear decreasing trends of metal concentrations in mussels. The lack of such trends was partially attributed to the short period covered by the studies. The main source of metal pollution in the WS is from river Scheldt and the industrial harbour of Antwerp upstream. Vertical and horizontal distribution of metals in the WS is greatly influenced by strong hydrodynamic and physico-chemical conditions prevailing in the estuary (Gerringa et al., 1996; Paucot & Wollast, 1997; Baeyens, 1998; Baeyens et al., 1998a, b, c; Garringa et al., 1998; Zwolsman & Van Eck, 1999). Physico-chemical factors are also responsible for physical and chemical partitioning behaviour and speciation of metals within and between different compartments. Consequently, changes in the bioavailability of metals to estuarine organisms may be as important as changes in total metal inputs and concentrations.
Seasonal variations have a potential to affect metal concentrations in estuarine organisms due to changes in physico-chemical variables and some biological factors. Seasonal effects are critical in biomonitoring programmes especially when sampling was done at different times of the year. In the WS, Zwolsman et al. (1997) and Bordin et al. (1992) showed strong seasonal variations in river flow, dissolved oxygen, pH, temperature, salinity and suspended particulate matter. Consequently, seasonal variations in dissolved heavy metals in the WS are more pronounced compared to the nearby less-polluted, tidal basin of the ES (Gerringa et al., 1996, Zwolsman et al., 1997; Gerringa et al., 1998). Currently, little is known about the influence of seasonal changes on metal content in organisms in these areas. The only published study in the Scheldt estuary (Bordin et al., 1996a, b) on the bivalve Macoma balthica, showed high uptakes of Cd and, to a lesser extent, Cu in winter than in summer periods while Zn appeared to be constantly regulated. Unfortunately, the study has never been repeated in other species in the estuary. The objectives of the current study were; (i) to study both short-term (1996–2002) and long-term (1978–2002) temporal and spatial distribution of heavy metal concentrations in mussels in the WS in order to evaluate the impact of decreased pollution input into the estuary, (ii) to determine the influence of season on metal concentrations in mussels in a polluted (WS) and less polluted (ES) area.
Materials and methods Between 1996 and 2002, samples of wild mussels of 3–4 cm shell length were routinely collected from 4 sites in the Western Scheldt estuary (Fig. 1). The selected sites following both pollution and salinity gradients. The salinity at the sites ranged from 18 ppt at Hansweert at the upper limit of mussel distribution to full seawater with 34 ppt at Westkapelle near to the mouth of the estuary (Fig. 1). Samples for annual variation were collected during the summer months between July–September, in order to sample the mussels in the post-spawning period and also in order to make comparisons with JMP data. For seasonal variations, two sites were included in the study; Hansweert the most polluted site in
171
Figure 1. Map of Western Scheldt estuary and the Eastern Scheldt tidal basin (The Netherlands) showing the five sampling sites; 1. Hansweert, 2. Ellewoutsdijk, 3. Vlissingen, 4. Westkapelle and 5. Wemeldinge.
the WS and Wemeldinge in the relatively lesspolluted Eastern Scheldt. The two sites were selected in order to investigate whether seasonal variations were depended on the level of metal pollution in the environment. Samples were taken in October and December of 1999 and in February, April and August 2000. During sampling, 25–35 mussels were always collected from each site close to the water line during low tide. Samples were then transported on ice in a cool box to the laboratory. Each individual was cleaned and then dissected with a clean scalpel blade to separate the soft tissues from the shells. Soft tissues of each individual were then placed in a polypropylene vial. Samples were dried in the oven for 72 h at 60 °C, after which tissue dry weight was determined. About 5 ml of ultra pure concentrated (69%) HNO3 and 0.25 ml 27% H2O2 were added. Samples were digested by heating in a microwave oven during four consecutive steps of 5 min at 80, 160, 240 and 320 W. After digestion, samples were diluted by adding 30 ml Milli-Q water in each vial. Metal concentrations in the final solutions were determined by ICP-AES (Cu, Fe, Mn, Zn) and ICP-MS (Cd, Co, Cr, Ni, Pb). Yttrium was used as an internal standard to correct for interference from high-dissolved solids
arising from high salt content and tissue matrix effects. Samples of reference material of mussel tissue (CRM 278R, Institute of Reference Materials and Measurements, European Commission, Geel, Belgium) were always included with each batch of samples for verification of the measurements. Recoveries in the reference materials were checked against certified values and measurements were only accepted if the recoveries in the reference samples were within 10% of certified values (Table 1). For statistical analysis, annual tissue metal concentrations in mussels were analysed using a 2-way ANOVA with year and site as independent factors. 2-way ANOVA was also applied to test the effects of season and site on metal concentration in mussels. In the latter case, only two sites (Hansweert and Wemeldinge) were used in the analysis.
Results Spatial trends Results (Fig. 2 and Tables 2 & 3) showed that sites near to the sea had significantly lower concentrations of all the heavy metals studied. In the cases of
172 Table 1. Metal concentrations (lg/g dry weight) in certified reference mussel tissue (CRM 278) included in all batches analysed in 1996, 1999 and 2002 Metal
Certified (lg/g)
Measured (lg/g)
Recovery (%)
1996
1999
2002
Cd
0.35 (0.01)
0.35 (0.02)
0.36 (0.02)
0.35 (0.03)
Co
–
0.43 (0.08)
0.41 (0.07)
0.49 (0.01)
100–105
Cr
0.80 (0.06)
0.75 (0.04)
0.76 (0.03)
0.79 (0.09)
94–99
Cu
9.5 (0.2)
9.6 (0.1)
9.5 (0.2)
9.3 (0.9)
98–101
Fe
–
131 (1)
132 (3)
135 (4)
Mn
7.7 (0.2)
7.7 (0.1)
7.7 (0.1)
7.8 (0.2)
100–101
Ni Pb
– 2.00 (0.04)
0.62 (0.05) 1.96 (0.12)
0.60 (0.04) 2.0 (0.10)
0.63 (0.03) 1.95 (0.08)
97–100
Zn
83.1 (1.7)
79.3 (0.2)
79.0 (0.2)
80.2 (1.6)
95–97
SD is reported in brackets.
Figure 2. Evolution (1979–2002) of metal concentrations (lg/g) in mussel tissues at four sites in different sectors of the Western Scheldt estuary and one site in the Eastern Scheldt. Data for 1979–1992 was obtained from JMP of the Netherlands (Luten et al., 1986; Stronkhorst, 1992). The 1978–1992 data are pooled measurements of 50 individuals while 1996–2002 values are means of 25–35 individual with standard deviations as error bars.
Cd, Ni, and Zn, concentrations at Hansweert in the upper part of the estuary at salinity 15–19 ppt (due to tidal cycle), were about an order of mag-
nitude higher compared to Westkapelle on the seaside at salinity 34 ppt. When the WS and ES were compared, 2-way ANOVA (Table 4) showed a
173 Table 2. Emission estimates for selected heavy metals from Belgium (BE) and The Netherlands (NL) for the years 1985 and 1999/2000. The differences between the two periods are expressed as percentages of the 1985 values Metal
Country
Discharge
(kg/year)
Reduction
to water
1999
(%)
Table 3. Results of a 2-way ANOVA for the effects of ‘site’ (pollution and salinity gradients), ‘‘year’’ and interaction between the two factors on metal concentrations in mussels in the WS Element Source of
d.f.
MS
F-ratio
p-value
variation
1985 Site
3
3049
327.34
