Study of the Effect of Chemical Pollution with Coal-Fired Power Plant on the Fish of Lake Kenon (Trans-Baikal Territory, Russia)

Lake Kenon is situated in the limits of the city of Chita, Transbaikal Territory, and located at latitude 52°04.362' N and longitude 113°21.432' E at an altitude of 653 m a.s.l. (Fig. 1). The catchment area of the lake is 227 km², the surface area is 16 km², the average depth is 4.4 m, the largest depth is 5.2 m, the length is 5.7 km, the average width is 2.8 km and the shoreline length is 17.4 km (Itigilova et al. 1998). Lake Kenon is a natural lake of the Amur River basin. Lake Kenon is used as a cooling pond for TPP-1 since 1965. Some abiotic indicators of Lake Kenon are shown in Figure 2. According to these data, Lake Kenon is a fresh-water body with an average level of salinity (TDS = 548 ± 25.1 mg L⁻¹). pH values indicate alkaline conditions and with a sufficient amount of dissolved oxygen. Hydrocarbonate composition of surface and underground waters is typical for these zonal and climatic conditions (Zamana et al. 1998, Zhuldybina 2010, Zamana et al. 2011). The hydrochemical composition of lake waters from a two-component – sodium hydrogen carbonate until the 60s of the last century was transformed into a three-component – sulfate-hydrocarbonate-chloride sodium-calcium-magnesium (Tsybekmitova 2016, Usmanova et al. 2018) (Table 1). The water composition change was due to the ash dump leakage. Approximately, 2.2–2.4 thousand tons of sulphates enter the lake annually (Zhuldybina 2010).

Fig. 1

Fig. 2

In the present report, we investigate species dominant in the fish community of Lake Kenon – Carassius auratus gibelio (Bloch 1782) and Perca fluviatilis (Linnaeus 1758). The long-continued catch rate for these fishes averaged not less than 80% of the total catch. Samples of fish were collected during field investigations performed from 2014 to 2016 using set nets within 3 h of fishery operation. Fish catch areas are shown in Figure 1. Table 2 represents particular characteristics of the selected species of both genders without conspicuous morphological changes. Fish are the final link in the food chain in the water ecosystem. We took this into account for the study of the migration of chemical elements along the trophic chain. Therefore, a preliminary analysis of food components of the fishes was carried out, and it was established what each species under study to food upon on the day of sampling. We used these data to construct diagrams of food chains. Given the fact that the fish in Lake Kenon is used in human nutrition, considerable attention has been paid to the study of the accumulation of chemical elements in the muscles of fish.

Immediately after collection, fish samples were put in a clean polythene bag to transport the fish samples to the laboratory of the Institute. In the laboratory, captured ichthyologic material was immediately analysed: each fish sample under study was identified to species and their lengths and weights were measured. Afterwards, the ages of the fishes were determined by interpreting sampled scales. The samples of fish muscle and food components were washed with distilled water and were cut into small pieces (2–3 cm), were then air-dried to remove the extra water and were then oven-dried until the constant weight was obtained. Samples were subsequently sent to the laboratory of the Institute of Microelectronics Technology and High-Purity Materials of the Russian Academy of Sciences (Chernogolovka, Moscow, Russia). Chemical elements in samples were determined by atomic emission spectrometry (iCAP-6500, Thermo Scientific, USA) and mass spectrometry (X-7, Thermo Elemental, USA). All samples were analysed for the presence of Cr, Mn, Cu, Zn, Pb and total Hg. These chemical elements are of the greatest concern in toxicology (Spry, Wiener 1991, Pandey, Madhuri 2014), although Cr, Mn, Cu and Zn are essential for normal physiological processes (Heath 2002). The accuracy of the analytical procedure was checked by the analyses of certified reference materials: for water – Certified Reference Material “Trace Metals in Drinking Water”; for bottom sediments – Certified Reference Material No. 521-84Ï “SGD-1A”, Essexite; for fish material – muscle tissue of Perca fluviatilis (Linnaeus, 1758) from Lake Baikal (SRM, Baikal perch tissue, BOk-2, registration number COOMET CRM 0068-2009-Ru). The results of the analysis of standard reference materials (BOk-2) and certified values of the elements are depicted in Table 3.

We used two factors to evaluate the chemical element concentrations in fish: the bioaccumulation factor (BAF) and the trophic magnification factor (TMF). The chemical element concentration was compared with the maximum permissible limits (RF) and EPA (US) standards. BAF was used to evaluate the chemical element concentrations in fish tissues and was calculated as the ratio of the concentration of pollutant (chemical elements) accumulated in the tissue of organism with respect to the concentration of chemical elements in surrounding water using the following formula (Jezierska, Witeska 2001, Van der Oost et al. 2003): BAF=Cfish/Cwater {\rm{BAF}} = {{\rm{C}}_{{\rm{fish}}}}/{{\rm{C}}_{{\rm{water}}}} where: –

C_fish is the concentration of chemical elements in fish tissue mg kg⁻¹,

If BAF is greater than or equal to 1, biological objects tend to accumulate metals.

As consumption and accumulation of a greater part of chemical elements in fish mainly result from feeding, we analysed the level of metal in the stomach content (food components). We calculated TMF to interpret the results of chemical element accumulation in trophic levels of the ecosystem. TMF reveals the relationship between the chemical element concentration in predator and the chemical element concentration in prey. The equation is as follows (Dobrovolsky 2003): TMF=Cpredator/Cprey {\rm{TMF}} = {{\rm{C}}_{{\rm{predator}}}}/{{\rm{C}}_{{\rm{prey}}}} where: –

C_predator is the concentration level of chemical elements in the organism or organ of predator,

The findings on chemical elements content in fish tissues were analysed with Microsoft Excel 2010 and STATISTICA 10 for Windows (Copyright © StatSoft, Inc). The statistical significance was set at p < 0.05. Principal component analysis (PCA) was used to perform statistical treatment of the data and to reveal the most common patterns of the relationships between the particular species and the elements accumulated in different tissues. Normalised data were obtained by dividing the observed values by the root-mean-square deviation (Shipunov et al. 2014).

Previous studies showed that the ash dump leakage, rich in S, Cr, Mn, Cu, Zn, Hg and Pb, flows into Lake Kenon (Tsybekmitova 2016). Table 4 shows the contents of chemical elements in the aquatic environment. Our investigation revealed that water contained low concentrations of the studied metals. With the exception of copper, the trace metal concentrations in water did not exceed EPA, but Cr and Hg were compared to national standard MPL (Table 4). The contents of the other chemical elements fell below MPL and varied (mg L⁻¹): Cr (from 0.7 to 1.5), Mn (from 2.3 to 6.8), Zn (from 1.6 to 4.0) and Pb (from 0.29 to 2.6). The comparison of received mass concentrations of chemical elements with Clark's value for sedimentary rocks revealed that bottom sediments in Lake Kenon contained low concentrations of the studied metals (Table 4).

The feed preferences of the dominant fishes in Lake Kenon are shown in Figure 3. P. fluviatus mostly inhabit the littoral area of the lake with abundant vegetation. Being a benthophagous fish, it can occupy the trophic level of predators. The greater part of its ration during the period of our research consisted of fish larvae (80%). C. auratus gibelio is a benthic species mainly feeding on plant remnants (charophytes) and detritus (sums up to 85%). The concentrations of chemical elements in the food components of the examined fishes are represented in Table 4. Chromium, magnesium and lead levels in Chironomus spp. and Chara sp. were higher than in amphipods. Copper and mercury levels were higher in amphipods than in other organisms. The amphipods too have a high level of mercury.

Fig. 3

The concentrations of heavy metals in muscles and food bolus are shown in Table 5. In the muscles of P. fluviatus and C. auratus gibelio, the contents of chemical elements in descending order are as follows: Zn > Cu > Mn > Pb > Hg > Cr. In the muscles of P. fluviatus, the contents of Mn, Cu and Zn are insignificant as compared to the level of chemical elements in food components. The concentrations of Mn and Pb in the muscles researched fish species are close to the MPL but higher than the EPA requirements, and the Hg concentration exceeds the MPL. In the muscles of C. auratus gibelio, the contents of Mn and Hg correspond to MPL, but higher than the EPA requirements, whereas the level of Zn is much higher than MPL and EPA. The concentrations of Cr, Cu and Pb fell below MPL. Higher contents of chemical elements in C. auratus gibelio are due to its benthic habitat, and there was total accumulation of chemicals from water, bottom sediments and consumed food. High levels of metal in the stomach content of the fishes were detected in the following descending order: in P. fluviatus – Mn > Zn > Cu > Hg > Pb > Cr; in C. auratus gibelio – Zn > Mn > Cu > Cr > Pb > Hg.

The levels of chemical elements in the water, bottom sediments and food organisms from the stomach in dominant fishes are shown in Table 4. BAF and TMF for the fishes were calculated from those values (Figs 4 and 5). BAFs of chemical elements accumulated from the surrounding water for P. fluviatus in descending order are as follows: Zn > Pb > Hg > Cu (Fig. 4). P. fluviatus accumulates Hg in equal measure from both water and bottom sediments. BAFs of chemical elements accumulated from the surrounding water for C. auratus gibelio in descending order are as follows: Zn > Pb > Hg > Cu. Manganese and mercury are accumulated in the muscles of C. auratus gibelio from bottom sediments. The factors of trophic magnification chemical elements in the hydrobints of Lake Kenon are as follows (Fig. 5): the highest accumulation ratio Zn in C. auratus gibelio from Chara sp. (24 times) and Hg from Chironomus spp. (38 times). The highest accumulation ratio Zn (26 times) and Hg (29 times) at P. fluviatus from amphipods. At the same time, Hg in P. fluviatus muscles is more higher accumulated from Chironomus spp. (67 times). These results show that chemical elements enter organisms not only through the environment but also with food. For such elements as Cr and Cu in the trophic chains considered, it is not always obvious, which requires additional analysis.

Fig. 4

Fig. 5

Component analysis singled out two factors that totaled up to 69.84% (Fig. 6). Other factors were considered being insignificant in total variance. PCA revealed the following characteristics of the metal–species correlation. In the muscles of P. fluviatus, significant correlation on the principal component 1 (Axis F1) was with Hg (−0.79) and Pb (−0.55); in C. auratus gibelio – with Zn (0.93), Cr (0.74), Cu (0.74) and Mn (0.62). The principal component 2 showed a significant correlation of P. fluviatus with Pb (−0.69). Thus, the PCA diffraction analysis carried out practically confirmed the obtained results of chemical pollutantion of the corresponding studied fish.

Fig. 6

Our investigation revealed that water and bottom sediments in Lake Kenon contained low concentrations of the studied metals. Although in Lake Kenon, Hg exceeds the background value more than three times, which is comparable with polluted waters. The background values of the concentration of Hg in freshwater bodies of European and Caucasian Russia, and in those of the Tien Shan Mountains, were evidenced in the study by Nikanorov Zhulidov (1991) and estimated as equal to or less than 0.05 mg L⁻¹. The research (Chale 2002) has shown that concentrations of trace metals of water were lower than that in fish tissues, which is consistent with our research. The self-cleaning ability from water ecosystems where aquatic organisms a purify waters polluted plays a role here (Moiseenko et al. 2005, Alimov et al. 2013). As compared to the aquatic environment, the contents of chemical elements in bottom sediments are an order of magnitude higher (Table 4). Such a high concentration in bottom sediments by the fact that metals are bound to organic compounds of plant and animal residuals settling in bottom sediments (Duan et al. 2014). Correlations between chemical elements and organic matter of bottom sediments are well traced in Lake Kenon (Tsybekmitova et al. 2019). Due to the sedimentation of suspended organic matter capable of adsorbing ions and mineral particles from water, the bottom sediments of Lake Kenon are enriched with Mn, Zn, Hg and Pb. Bottom sediments not only function as accumulators of heavy metals but also as one of the potential sources of pollution of the chemical element ecosystem.

The feed preferences of the dominant fishes of Lake Kenon are as follows: P. fluviatus is benthophagous (Amphipods and Chironomus spp.) but can occupy the trophic level of predators. In research studies performed by Craig (1978), Dörner et al. (2003), invertebrates and age-0 fish were also the main food components of large P. fluviatus. C. auratus gibelio is a benthic species mainly feeding on plant remnants (Charophytes) and detritus (sums up to 85%). As indicated (Szczerbowski 1996), the most frequent diet items to C. auratus gibelio include planktonic crustaceans, insect larvae, molluscs and plants. Peňaz and Kokeš (1981) reported 100 and 91.3% of the fish from reservoirs of Sturovo and Chlaba to contain detritus in their digestive tracts. In this way, the C. auratus gibelio diet items in our study were similar in composition to those reported by other authors.

In such reference ecosystems as Lake Baikal, the content of Cr in the muscles of fishes ranges from 0.3 to 0.86 mg kg⁻¹ (Vetrov et al. 1989); in the ecosystem of Lake Kennebec (Maine, USA), the level of Cr in the muscles of P. fluviatilis ranges from 0.1 to 1.7 mg kg⁻¹ of dry matter (Friant et al. 1979), which was compared to our findings. Low concentration of Cr in the muscles of fishes is due to its higher accumulation in the systems of active metabolism (Moiseenko et al. 2005). In the fish muscles in Lake Kenon, zinc is 2–4 times higher, and Cu is seven times lower, and are comparable in Pb content to those obtained (Ebrahimpour et al. 2011, Younis et al. 2015). Hg accumulated in the muscles of C. auratus gibelio and P. fluviatus in Lake Kenon is higher than in Lake Chany and the Chivyrkuisky Gulf of Lake Baikal (Popov, Androsova 2008) and corresponds to the level of industrial impact on water bodies (Nyukkanov 1996, Pastukhov 2012). In the muscles of the fishes in Lake Kenon, the content of Zn is 2–5 times as high as in Lake Chany (Popov, Androsova 2008), which corresponds to the data of the Votkinskoye Reservoir (Gileva et al. 2014) and of the wetland ecosystem from the Lower Prut Floodplain Natural Park in Romania (David et al. 2012). Metals like Mn function as a cofactor in several enzyme systems. However, when in excessively high concentration, these bioactive metals may pose serious threats to normal metabolic processes (Bury et al. 2003). The content of manganese in the muscles of fish from Lake Kenon is lower than that presented in the work (Rahman et al. 2012), which might be due to the tendency of various species of fish to concentrate certain elements in their tissue more than the surrounding. In the food components of the fish stomach in Lake Kenon, the high concentration of Zn, Mn and Hg shows that chemical contaminants enter organisms not only through the environment but also with food, which is supported by research (Wang et al. 2015). For example, it was detected that approximately 70% of methylated Hg is consumed with food, while only 10% is accumulated through gills (Heath 2002).

On the biogeochemical barrier, the migration of chemical elements drops drastically and their concentrations begin to rise (Alekseenko 2003). At the same time, chemical elements flowing into water ecosystems are selectively accumulated in organisms through the system of trophic interrelations. In the plant food organisms (Chara sp.), chemical elements accumulation mainly originate from the water column (Cardwell et al. 2002, Bazarova 2013). Only manganese accumulates in them from bottom sediments. The detected content of Mn in bottom sediments (33 mg kg⁻¹, Table 4) is six times higher in the muscles of C. auratus gibelio (Fig. 4). Being transferred along the trophic chain, Mn is actively precipitated on the oxygen barrier made up by aquatic vegetation and breathing vibrations of Chironomus spp. larva (Nikanorov, Zhulidov 1991). From Chara sp. most of the chemical elements accumulate in C. auratus gibelios since is benthic species mainly feeding on plant remnants (charophytes) (Szczerbowski 1996). Also, food relations of C. auratus gibelio is connected with bottom organisms that inhabit in charophytes – with Chironomus spp. (Fig. 5). This results in higher contents of Hg, Cu, Zn in C. auratus gibelio in Lake Kenon as compared to P. fluviatus. Quantification analyses of chemical elements in fishes performed by a number of scientists (Sani 2011, Hashim et al. 2014, Nzeve et al. 2014, Moiseenko, Gashkina 2020) revealed a higher level of metals contamination in predators. The findings on the contents of chemical elements in P. fluviatus of Kenon Lake, shown as a predator, and on the contents in muscles of mercury and lead are higher than in C. auratus gibelios. The phenomenon of higher accumulation of Hg in predatory fishes as compared to non-predatory ones is explained by the progressive accumulation in the trophic chain typical for this metal (magnification effect) (Popov 2002, Komov et al. 2004, Popov, Androsova 2014). The food spectrum of P. fluviatus includes not only fishes but also bottom organisms. As it was observed, Zn and Hg in bottom sediments through amphipods and Chironomus spp. reach fishes while accumulating in them exponentially (Fig. 5). Nazyrov (2003) detected the correlation between zoobenthos (especially Chironomids larva) and bottom sediments, which contributes to the accumulation of Zn and Hg. It was observed that the Pb enters fish through water containing high concentrations of metals (Wood et al. 2012). Consequently, high concentrations of Pb in the aquatic environment, Pb to accumulation in aquatic organisms. In Lake Kenon, Pb enters the body of P. fluviatus from benthic organisms, and into C. auratus gibelios – from Chara sp. and Chironomus spp.