Dec 17, 2011 - northern pike Esox lucius, pike perch Sander lucio- perca, wels catfish Silirus glanus, common carp. Cyprinus carpio, European eel Anguilla ...
Environ Monit Assess (2012) 184:6553–6561 DOI 10.1007/s10661-011-2440-9
Biomonitoring of polychlorinated biphenyls (PCBs) in heavily polluted aquatic environment in different fish species Tímea Brázová & Vladimíra Hanzelová & Dana Miklisová & Danka Šalgovičová & Ľudmila Turčeková
Received: 4 May 2011 / Accepted: 2 November 2011 / Published online: 17 December 2011 # Springer Science+Business Media B.V. 2011
Abstract The distribution and concentrations of polychlorinated biphenyls (PCBs) were determined in fish species (European perch Perca fluviatilis, northern pike Esox lucius, pike perch Sander lucioperca, wels catfish Silirus glanus, common carp Cyprinus carpio, European eel Anguilla anguilla, freshwater bream Abramis brama, goldfish Carassius auratus, and roach Rutilus rutilus) in a heavily polluted water reservoir Zemplínska šírava (Slovakia). The study performed at two different time points 5 years apart (2004 and 2009) revealed serious PCB contamination of fish muscle tissue and significant interspecies as well as tissue-specific differences in PCB uptake by fish. Total PCBs broadly correlated with the trophic position of individual fish species within a food chain (P0.05). The study has shown that the kind of fish, its feeding habit, and specific conditions of the habitat are mutually interrelated factors that are responsible for significant variations in fish body burdens. A tendency to PCB biomagnification was also proved in some fish species of this water reservoir. Keywords Polychlorinated biphenyls . Fish . Zemplínska šírava water reservoir . Pollution
Introduction Polychlorinated biphenyls (PCBs) are highly persistent compounds in the environment, especially in water sediments that represent a long-lasting reservoir from which PCBs may continue to be released over a long period of time, because of their low solubility in water and low volatility (EPA 1999). The involvement of PCBs in the food chain occurs through incorporation of suspended particles by phytoplankton and zooplankton, taking place at the beginning of the food chain. Consecutively, bottom feeders and other
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aquatic organisms ingest and accumulate PCBs upward in the food chain (Larsson et al. 1990; German and Zakonnov 2003). Some fish species are at the top of the food pyramid in an aquatic ecosystem, thus bioaccumulating in the highest levels of PCBs. Bioaccumulation of PCBs is a complex phenomenon, controlled by numerous physiological and environmental factors (McIntyre and Beauchamp 2007). The extent of PCB accumulation differs from species to species due to differences in the diet and metabolic processes, the age, size, season, sex, and physiological condition of the animal (Drouillard et al. 2001), and their influence on the PCB level is not yet entirely coincident. It is commonly accepted, however, that food is the dominant uptake pathway when considering less hydrophilic contaminants such as PCBs (Borgå et al. 2004). Since 2004, we have studied PCB accumulation and tissue-specific PCB distribution in fish from Zemplínska šírava water reservoir (eastern Slovakia; Fig. 1), which qualifies as one of the most PCBFig. 1 Location of the sampling sites in the Zemplínska šírava water reservoir
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contaminated places in Europe (Kočan et al. 2001; Šalgovičová and Zmetáková 2006). Due to the past production of chemical factory located in the nearby town of Strážske, the huge amount of PCB compounds was released to the reservoir without any treatment (decontamination) and preventive measures that resulted in heavy contamination of soil, superficial, and underground waters and subsequently food chains in this area (Langer et al. 2003). Hence, the PCBs in the Zemplínska šírava reservoir and inflowing Šíravský canal belong to the so-called old environmental burdens and their amount fluctuates from tens to hundreds of milligrams per kilogram of sediment dry weight, and it is assumed that at least 40,000 tons of PCB-contaminated sediments are still present in the water reservoir (Dercová et al. 2008). Several studies over the past 20 years have indicated that elevated concentrations of PCBs in the reservoir are a potential hazard to human and aquatic health (Kočan et al. 2001; Petrik et al. 1991). To help address these concerns, a more detailed study of the six NDL indicator PCB congeners
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(IUPAC nos. 28, 52, 101, 138, 153, 180) was initiated (T. Brázová, personal data), and it was already possible to detect that concentrations of PCBs in muscle tissue of fish significantly exceeded the MRL established for fish in the Slovak Republic (Food Codex of the Ministry of Agriculture of the Slovak Republic 2006). The aim of the present study was to determine species-specific accumulation of PCBs by considering trophic habits, position in a food web, and weight of various fish species from the water reservoir Zemplínska šírava at two different time points 5 years apart. A closer aim was to assess tissue-specific PCB concentrations in the muscles, liver, kidney, and brain of predatory and non-predatory fish.
Material and methods Study site In the years of 2004 and 2009, monitoring of PCBs in fish was carried out at eight sampling sites of the PCB-contaminated water reservoir Zemplínska šírava, eastern Slovakia (Fig. 1). Zemplínska šírava water reservoir (48°47′32″ N; 22°0′42″ E) is one of the biggest artificial water storages in Slovakia located in the eastern part of the country (Fig. 1). It was built between 1961 and 1965 for a flood run-off regulation at the Laborec River and partly for irrigation purposes in the territory. The length of the reservoir is 11 km, Table 1 Number of examined fish species with indication of their food items and the trophic level
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its width about 3.5 km, and it covers an area of 33 km2. During past production of a chemical factory in Strážske, the PCB compounds were released throughout Strážsky (effluent) canal to the Laborec River and from there by Šíravský (influent) canal to the Zemplínska šírava reservoir (Fig. 1). Ichtyofauna of the reservoir is abundant, represented by dense populations of common carp, Cyprinus carpio L.; bream, Abramis brama (L.); pikeperch, Sander lucioperca (L.); pike, Esox lucius L.; perch, Perca fluviatilis L.; wels catfish, Silurus glanis L.; and goldfish, Carassius auratus (L.).
Fish collection Altogether 50 fish of nine species and five families (Anguillidae, Cyprinidae, Esocidae, Percidae, and Siluridae) were collected. Fishes were transported to the laboratory alive, weighted, measured, and divided into individual feeding guilds (Baruš and Oliva 1995; Froese and Pauly 2011) (Table 1). Tissue samples taken from fish were stored at −20°C until further processing. In 2004, only muscle tissues (19 samples) were collected. The more detailed study, focused on tissuespecific distribution of PCB fish from this locality, was performed in 2009 to help assess the temporal variation of PCBs in the reservoir using the analyzed fish species. In addition to muscles, samples of the liver (hepatopancreas in cyprinids), kidneys, and brain were taken from 31 fish belonging to eight species. In
Fish species
N
Major food item
2004
2009
Trophic levela
Predators European perch—Perca fluviatilis
0
16
Zoobenthos, necton
3.2–4.4
Northern pike—Esox lucius
1
2
Necton
3.8–4.5
Pike perch—Sander lucioperca
2
3
Necton
4.3
Wels catfish—Silurus glanis
0
3
Necton
4.3–4.4 2.1–3.1
Non-predators
N number of examined fish a
Trophic level was assessed according to Froese and Pauly (2011)
Common carp—Cyprinus carpio
2
1
Zoobenthos
European eel—Anguilla anguilla
7
0
Zoobenthos
2.3–3.5
Freshwater bream—Abramis brama
5
1
Zoobenthos
2.9–3.1
Goldfish—Carassius auratus
1
5
Zoobenthos
2.0
Roach—Rutilus rutilus
1
0
Zoobenthos, plants
2.3–3.4
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perch, in which small-sized individuals prevailed, organs and tissues were pooled by the weight of fish as followed: Individuals weighting up to 10 g (n=7), 14–30 g (n=5), and four remaining fish with the weight of 60–130 g were analyzed separately. The scientific and common names of fish were used according to the FishBase database (Froese and Pauly 2011); major food items of fish as well as their trophic levels were stated by Baruš and Oliva (1995) and Froese and Pauly (2011).
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analyzing differences in PCB loads between years. The effect of the different trophic strategies in predatory and non-predatory fish on PCB levels in the individual tissue samples, respecting the number of observations, was tested with nonparametric Mann–Whitney U test or Kruskal–Wallis ANOVA with post hoc multiple comparing (Siegel and Castellan 1988). The correlation between PCB load and body weight of fish was tested by Pearson’s correlation coefficient. The analyses were performed in Statistica for Windows, version 9.0 (StatSoft, Inc. 2009).
Analytical procedure With slight modifications, the method described by Himberg et al. (1987) and Fisher and Ballschmiter (1989) was applied for extraction and cleanup of the samples. Fish samples were homogenized with anhydrous sodium sulfate and extracted with a mixture of petroleum ether (90%) and acetone (10%) using a separation funnel. The extract was concentrated using a rotary evaporator, subsequently purified using a Florisil chromatographic column according to STN EN 12393-2 (2001). The final extracts were analyzed on a Hewlett-Packard 6890 gas chromatograph equipped with electron capture detector. The capillary column was 30 m, 0.25 mm i.d., and 0.25 μm film thickness HP-5. GC parameters were injector temperature 250°C, detector temperature 300°C, and carrier gas helium with flow rate 1.4 ml/min. The following oven temperature program was used: start temperature 80°C for 1 min, 80–180°C at 30°C/min held for 1 min, 185– 205°C at 6°C/min held for 15 min, and 205–290°C at 20°C/min held for 7.5 min. Individual PCB congeners were identified based on the retention times of a known standard and qualified by comparing the peak area to the appropriate peak in the standard mixture (PCB Mix CSCA-06). The extract was injected under splitless mode. The recovery rates of PCBs in spiked samples were between 80% and 95%, whereas the detection limits were 1 μg/kg on a wet weight basis. Six PCB indicator congeners, PCB 28, 52, 101, 138, 153, 180, were examined. All PCB concentrations in biological samples are given in milligrams per kilogram lipid weight. Statistical analysis If the data obtained did not meet the requirements for parametric statistical tests (normality), they were analyzed non-parametrically. The t test was used for
Results PCB distribution related to fish species Comparison of the total PCB concentrations (∑ of six PCB congeners) measured in muscle tissues of nine fish species collected in 2004 and 2009 from the Zemplínska šírava water reservoir varied greatly among species (Fig. 2). In both time points, the concentrations were particularly high in predatory fish species, perch, pike, and pike perch; however, comparable PCB values were also found in nonpredatory freshwater bream (in both sampling periods) and roach (in 2004). Within past 5 years, a tendency to bioaccumulation was clearly demonstrated in some species (freshwater bream, pike, pike perch) (Fig. 2). In general, PCBs in muscle tissue of these fish from the reservoir went up approximately two times during five consecutive years, and this increase was statistically significant (t=−2.43, df=13, P
