Crustaceans as biological indicators of heavy metal pollution in Lake ...

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Abstract. Trace metals (Cd, Cu, Pb, Zn) were measured in mixed zooplankton samples collected from the open water of Lake Balaton (Hungary) in order to ...
Hydrobiologia 506–509: 359–364, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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Crustaceans as biological indicators of heavy metal pollution in Lake Balaton (Hungary) Anna Farkas, J´anos Sal´anki & Istv´an Varanka Balaton Limnological Research Institute of the Hungarian Academy of Sciences, Tihany, Hungary E-mail: [email protected] Key words: biomonitoring, zooplankton, heavy metals, Lake Balaton

Abstract Trace metals (Cd, Cu, Pb, Zn) were measured in mixed zooplankton samples collected from the open water of Lake Balaton (Hungary) in order to assess spatial and seasonal changes in the heavy metal load of different sites, during 1996–2000.Samplings were performed usually twice a year in different seasons (spring, summer and autumn). The heavy metal concentrations of zooplankton biomass were determined by atomic absorption spectrophotometry. Additionally, for some of the sampling sites – Western- and Eastern basins – the correlations between the heavy metal load of Crustaceans and the element concentrations of the water recorded monthly by the Transdanubian Environmental Protection Agency were also analyzed.The average metal concentrations in zooplankton varied in the following ranges: Cd: 0.25 – 3.91; Cu: 5.9 – 26.4; Pb: 1.59 – 12.84; Zn: 37.6 – 180.5 mg kg−1 dry weight. Significant spatial and seasonal variations with occasionally outstanding differences in the heavy metal load of samples could be observed during the investigated period. The heavy metal load of the Crustacea plankton biomass in summer and autumn proved to be usually higher than in spring. During the investigated period an overall significant increase in the cadmium, copper and lead load of the Crustacea plankton populating the lake could be observed. Pearson correlation analysis performed between the heavy metal concentration of Crustacea plankton biomass and that of the water in the two outlying basins of the lake revealed strong relationship for Cd, Cu and Zn, while for lead the correlation proved to be not significant.

Introduction The long-term monitoring of anthropogenic pollution in aquatic ecosystems is of environmental and human health concern even nowadays, when numerous effective measures were undertaken to reduce the pollution impact of natural water bodies. In these studies aquatic organisms are widely used for biological monitoring of variations in the environmental levels of anthropogenic pollutants (Phillips, 1980; Hellawell, 1986). Among aquatic indicator organisms a significant role is assigned to zooplankton assemblages due to their significant capacity to accumulate heavy metals, and their essential role in the enrichment of anthropogenic compounds in food chains (Prosi, 1981; Stemberger & Chen, 1998). Interest in monitoring the anthropogenic pollution of Lake Balaton is justified, because the lake and its watershed are loaded by a moderate nutrient load

and a slight pollution of heavy metal, caused besides natural, geological sources mainly by industrial and agricultural works located in the catchment (Müller, 1981; Czégény et al., 1984; Herodek et al., 1995; V.Balogh et al., 2003). The anthropogenic heavy metal input originates mainly from local municipal sources, waste deposits, the heavy road and rail traffic along the 210 km long lakeshore, from boating and atmospheric deposition (Hlavay et al., 1999). On average, the concentration of dissolved heavy metals of inflow waters, which provide more than half of the water budget of the lake, vary nowadays in the following ranges: Cd 0.1 – 2.8; Cu 1.1 – 8.9; Pb 0.5 – 8.3; Zn 12 – 74 µg l−1 . The total heavy metal concentration of aerosols in the catchment measured for example in 1997 was as follows: Cd 0.55 – 0.74; Cu 3.8 – 4.9; Pb 26.4 – 29.8; Zn 8.7 – 37 ng m−3 (Hlavay et al., 1999).

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Figure 1. Geographical position of Lake Balaton and the location of sampling sites.

In this paper we present the spatial and seasonal variations in the load of four heavy metals (Cd, Cu, Pb, Zn) in zooplankton samples during 1996 – 2000, and the links detected between metal levels in zooplankton and metal concentrations in the water of two study areas: the Eastern-, and Western-basin of Lake Balaton (Fig. 1). The heavy metal concentrations in the water were measured by the Transdanubian Environmental Protection Agency in a parallel study within a time interval not longer than 3 weeks.

lected by towing a plankton net (mesh size 200-µm) from about 0.5 – 1 m depth to the water surface. This sampling technique was chosen to ensure the collection of crustacean plankton consisting almost exclusively of mature stages of copepods (>95%). The species composition of zooplankton samples were randomly checked by sampling sites, i.e. in one of the three replicates prepared from each sample. Zooplankton samples designated for heavy metal analysis were briefly rinsed with double-distilled water, dried on good quality filter paper and cleaned of solid impurities (paint particles, tar lumps, rust) under close visual examination. Subsequently, the samples were dried at 60 ◦ C, weighed, and subjected to wet digestion in an open system with a mixture of 65% HNO3 and 30% H2 O2 (Krishnamurty et al., 1976; Farkas, 1993). Metal concentrations of zooplankton samples were determined with a Perkin-Elmer 5100 PC atomic absorption spectrophotometer equipped with an HGA 60 graphite furnace and using deuterium arc background correction. Multiple spatial and seasonal contrasts of mean metal concentrations in zooplankton were studied with the Student-Newman-Keuls test, while Pearson correlation test was used to check for significant relationships between metal levels in zooplankton and metal concentrations in the water.

Materials and methods Results Lake Balaton located at the western part of Hungary is the largest shallow lake in Central Europe (Fig. 1). The surface area is 596 km2, the mean depth 3.25 m and the volume 1.9 109 m3 . The inflow waters and the processes taking place within the lake control the chemical features of the lake water. Limestone and dolomitic rocks predominate in the catchment area, so that the waters discharged to the lake carry Ca2+ , Mg2+ and HCO3 − in high concentrations. Owing to CO2 exchange with the atmosphere and to photosynthesis, large volumes of CaCO3 are present in the lake. Due to its high alkalinity and carbonate content the lake water does not contain heavy metals in ionic form. However in unfiltered water detectable toxic heavy metal concentrations can be measured due to their presence in inorganic and organic forms or adsorbed to colloid particles. Samplings of Crustacea plankton were performed usually twice a year in different seasons (spring, summer and autumn) at 15 sampling sites designated along five transects of the lake (Fig. 1). Plankton were col-

Copepods were generally numerically predominant in the crustacean community of Lake Balaton during the whole investigation period. Their relative proportion in the open water varied between 81 – 92% and 93 – 97% in the littoral zone. Mainly four copepod species, 1 Calanoida sp. Eudiaptomus gracilis (Sars) and 3 Cyclopoida spp.: Cyclops vicinus [Uljanin], Mesocyclops leuckarti (Claus) and Acanthocyclops robustus f. limnetica [Petkovski] were present in the samples. Our results agree well with those of previous studies dealing with the species composition of the zooplankton community of Lake Balaton (Ponyi, 1975; Zánkai & Ponyi, 1986; Ponyi 1991; Parpalˇa et al., 2003). Metal concentrations detected in the zooplankton biomass were generally consistent with values previously reported for uncontaminated systems (Yan & Mackie, 1989; Chen et al., 2000), but elevated levels detected at some sampling areas were indicative of contamination (Table 1). In general Cd concentrations (0.37–1.85 µg g−1 dry weight) were rather low, except

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Figure 2. Elevated levels of heavy metals in zooplankton at different sampling sites of Lake Balaton. Sampling sites: a – close to the northern shoreline; b – along the middle line; c – close to the southern shoreline. Table 1. Metal concentrations (arithmetical mean) in zooplankton (µg g−1 dry weight) and standard deviation (SD) during 1996 – 2000 Sampling occasions

No of samples Cd

1996

1997

1998 1999 2000

May July September May July Oct. April August July April July

45 45 45 51 51 51 51 51 51 51 51

0.55 ± 0.15 4.22 ± 3.13 1.30 ± 0.21 0.88 ± 0.30 0.89 ± 0.44 3.11 ± 0.39 2.02 ± 0.66 3.01 ± 1.20 2.85 ± 0.78 3.91 ± 2.06 2.18 ± 0.60

for elevated levels (7.42–36.87 µg g−1 dry weight) detected on two occasions (July 1996 and April 2000) at some sampling sites from the Eastern basin (Fig. 2 A, B). Significantly higher concentrations were recorded for Cu (on average 3.7–12.5 µg g−1 dry weight) showing an excessive load (71.4–276.3 µg g−1 dry weight) in summer 1999 at a few sampling locations in the Western basin (Fig. 2 C). Pb concentrations of zooplankton varied between 0.65–2.10 µg g−1 dry weight, with somewhat higher elevation in July 2000 (5.07–9.96 µg g−1 dry weight) at sampling sites situated in the Western basin of the lake (Fig. 2 D). The Zn concentration of zooplankton varied usually between 37.0–70.0 µg g−1 dry weight, except the significantly

µg g−1 [arithmetical mean ± SD] Cu Pb 7.53 ± 2.07 5.91 ± 1.11 10.81 ± 1.82 10.12 ± 4.35 11.83 ± 4.17 10.96 ± 5.33 6.7 ± 1.49 18.05 ± 7.43 26.43 ± 17.72 12.55 ± 7.64 13.35 ± 5.64

2.82 ± 1.46 2.29 ± 0.63 1.89 ± 0.59 2.53 ± 1.14 2.93 ± 1.12 2.08 ± 0.56 1.59 ± 0.39 1.83 ± 0.41 3.39 ± 1.38 3.13 ± 1.54 4.01 ± 2.63

Zn 180.5 ± 58.4 133.7 ± 37.2 157.8 ± 24.7 37.6 ± 5.3 42.4 ± 6.8 70.6 ± 5.3 56 ± 14.2 82 ± 10.6 57.4 ± 17.4 50.9 ± 26.3 53.5 ± 20.2

higher elevation observed for the samples collected in 1996 (80.5 – 157.8 µg g−1 dry weight) (Table 1). The pattern of temporal variation in the heavy metal concentration of zooplankton was not statistically similar during the studied period when comparing SITES/SPECIES, however highest elevations for all four elements were characteristic in general in summer and/or in autumn (Table 1). Mean Cd, Cu and Pb concentrations of zooplankton averaged for the whole lake indicate a slight increasing trend during the four years period (Table 1). For the assessment of long term variations of the heavy metal load of Lake Balaton, we have compared our results with the heavy metal concentration data of zooplankton recorded twenty years

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Figure 3. Box plots of mean heavy metal concentrations recorded in zooplankton samples during 1978–1979 and 1996–2000. The ‘box’ height defines the inter-quartile range. The horizontal bar in the box is located at the median. The tails define the 95% confidence limits of the metal concentration data. Table 2. Pearson correlation coefficients (r) and levels of significance (p) for the relationships between the main metal concentrations in zooplankton and metal concentrations in the water Element

Cd Cu Pb Zn

Western basin r p 0.62964 0.70368 0.01547 0.92412

0.002 0.001 n.s.