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Article

Using Rutilus rutilus (L.) and Perca fluviatilis (L.) as Bioindicators of the Environmental Condition and Human Health: Lake Łańskie, Poland

1
Chair of Commodity and Food Analysis, University of Warmia and Mazury in Olsztyn, ul. Plac Cieszyński 1, 10-726 Olsztyn, Poland
2
The Stanisław Sakowicz Inland Fisheries Institute in Olsztyn, ul. Oczapowskiego 10, 10-719 Olsztyn, Poland
3
Department of Limnology and Fishery, Institute of Animal Breeding, Faculty of Biology and Animal Science, Wrocław University of Environmental and Life Sciences, ul. J. Chełmońskiego 38 c, 51-630 Wrocław, Poland
4
Department of Ichthyology and Aquaculture, Warmia and Mazury University, Al. Warszawska 117A, 10-701 Olsztyn, Poland
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2020, 17(20), 7595; https://doi.org/10.3390/ijerph17207595
Submission received: 15 September 2020 / Revised: 15 October 2020 / Accepted: 16 October 2020 / Published: 19 October 2020
(This article belongs to the Special Issue Fish as an Environmental Quality and Human Health Bioindicator)

Abstract

:
The aim of this study was to determine the mercury content and fatty acids profile in roach (Rutilus rutilus L.) and European perch (Perca fluviatilis L.) from Lake Łańskie (Poland). Mercury content was higher in the muscles than other organs in both species (p < 0.05). Mercury accumulates along the food chain of the lake’s ecosystem. The value of the bioconcentration factor (BCF) indicated that Hg had accumulated in the highest amounts in muscles and in the other organs as follows: muscles > liver > gills > gonads. The metal pollution index (MPI) and target hazard quotient (THQ) were below 1, which means that these fish are safe for consumers. The values of HIS, GSI and FCF indicators show that both species of fish can be good indicators of water quality and food contamination. There were few differences between fatty acid content in the muscles of perch and roach. Contents of fatty acids having an undesirable dietary effect in humans (OFA—hypercholesterolemic fatty acids) were lower compared to hypocholesterolemic fatty acids (DFA, i.e., the desirable ones). In addition, the lipid quality indices AI and TI in the muscles of fish were at 0.40 and 0.22 (perch) and at 0.35 and 0.22 (roach), respectively. On this basis, it can be concluded that the flesh of the fish studied is beneficial from the health point of view.

1. Introduction

The quality of the aquatic environment and its impact on the organisms that live in it, especially those that are subject to human consumption, rise serious concerns these days. Among the lake ichthyofauna, several species best indicate the quality of the reservoir. These include vendace (Coregonus albula L.), smelt (Osmerus eperlanus L.), bleak (Alburnus alburnus L.), perch (Perca fluviatilis L.) and roach (Rutilus rutilus L.) [1,2]. Two processes are used to assess the quality of both the reservoir and the fish based on their contamination, namely bioconcentration and bioaccumulation. The bioconcentration index (BCF) is used to estimate the contamination in trophic chains based on the information about pollutant concentration of substances in the body and in the external environment [2,3]. It usually differs among various pollutants and even within one species [2], and can take values between 0 and infinity [4]. According to Sauliutė et al. [3], the higher the index, the more intense the bioconcentration of metals in fish. Contrary to the bioconcentration process in fish, which involves the absorption of chemicals from water through the respiratory surface and/or the skin, another process called bioaccumulation addresses all exposure routes, including food ingestion. However, like BCF, the bioaccumulation factor (BAF) in fish is the ratio of the concentration of a chemical in the organism to its concentration in water [5,6]. According to Zeitoun and Mehana [7], this index is used to assess the concentration of heavy metals in various fish tissues. As already mentioned, both of these processes take place in the body and allow the determining of the quality of water and aquatic organisms in terms of mercury contamination. Mercury is accumulated in aquatic food chains and can undergo the biomagnification process, hence it can pose a threat to human health [8]. It is known that fish, as well as water mammals and waterfowl used as food sources, are important sources of mercury in some populations, especially those who eat fish or wild game from the top of the food chain (i.e., larger fish and larger mammals) [9].
Fish for human consumption are acquired from two main sources. One is the intensive breeding combined with artificial reproduction in captivity [10,11,12,13,14] and the other is fishing in oceans, seas, lakes and rivers. Fish farming, especially in recirculated aquaculture systems (RAS), is carried out under strict control of both the physicochemical parameters of water and food quality (e.g., [15,16]). However, in the wild, fish eat food that they find, which may contain contaminants that are harmful not only to the fish themselves, for example, by interfering with reproductive efficiency (e.g., [17]), but also potentially to humans who consume these fish. This is particularly important because accumulated deposits, including heavy metals, can be actively moved across the body of fish, especially during the development of gonads and gametes before reproduction, and their concentrations may change between different fish organs [18,19]. On the other hand, fish and fish products are ideal human food, because they are the source of minerals, vitamins, proteins and fatty acids, especially the long-chain n-3 polyunsaturated fatty acids [20,21]. The main functions of fatty acids include: great sources of energy—high energy per gram (37 kJ/g fat), and transportable forms of energy—blood lipids; storage of energy, e.g., in adipose tissue and skeletal muscle; component of cell membranes; insulating agents—thermal, electrical and mechanical insulation; and signaling molecules—eicosanoids and gene regulation (transcription) [22]. Apart from the fact that eating fish is part of the cultural traditions of many people [23], it is also known that the diet consisting of fish meat has many benefits for the human body, because it has the lowest level of saturated fatty acids (SFA), which are responsible for the increased incidence of cardiovascular diseases [24]. One of the factors of this disease is the elevated level of LDL cholesterol fraction [25]. According to Lunn and Theobald [25], replacing SFA with monounsaturated (MUFA) or polyunsaturated fatty acids n-6 PUFA reduces the level of LDL (“bad”) cholesterol. According to Djazayery and Jazayery [26], α-linolenic acid (ALA), eicosapentaenoic acid (EPA) and docosapentaenoic acid (DHA), representing n-3 polyunsaturated fatty acids (PUFA), play important roles, especially in the treatment of cardiovascular diseases and other hazards that affect human health and life. The same opinion is shared by other authors showing both the causes and effects of the low consumption of foods rich in these fatty acids [27,28,29,30,31,32,33,34,35,36].
Roach and perch are the indicator fish of Europe’s freshwater and brackish water. They live in many types of waters and can eat very diverse food, which makes them reflect the cleanliness of the environment they inhabit (e.g., [37,38,39]). The health benefits and risks are likely to vary according to the fish species and fish size, harvesting and cultivation practices, and the frequency and amount consumed and the way in which it is served [23,40,41]. Consequently, the aim of this study was to determine:
  • Differences between mercury content, hepatosomatic index (HSI) and gonadosomatic index (GSI) in two freshwater fish species examined.
  • Differences between mercury content in organs (muscles, liver, gills and gonads) of the same species.
  • The impact of biometric parameters (body weight and total length) and Fulton’s condition factor (FCF) on the content of mercury in selected organs of fish.
  • The health risk posed by mercury using estimated daily intake (EDI), tolerable weekly intake (EWI) and target hazard quotient (THQ).
  • Metal pollution index (MPI) and bioconcentration factor (BCF) based on the mercury content of the four organs.
  • Differences between the fatty acids profile and the lipid quality indices (atherogenicity index (AI), thrombogenicity index (TI), flesh-lipid quality index (FLQ), hypercholesterolemic fatty acids (OFA) and hypocholesterolemic fatty acids (DFA)) in muscles of perch (Perca fluviatilis L.) and roach (Rutilus rutilus L.).

2. Materials and Methods

2.1. Sampling and Sample Preparation

Perch (Perca fluviatilis L.) (n = 9) and roach (Rutilus rutilus L.) (n = 10) were caught from Lake Łańskie, which is located in the vast Ramuckie Forests, about 15 km south of Olsztyn. The lake is one of the largest and deepest lakes in the Olsztyn Lake District (northeastern Poland) (Figure 1), located in the Protected Landscape Area of the Wilderness Napiwodzko—Ramucka, Natura Areas 2000 PLB280007—Wilderness Napiwodzko—Ramucka and PLH28005—Refuge Napiwodzko—Ramucka. The area around the northeastern shore of the lake is one of the largest forest reserves of the voivodeship, called Warmiński Forest. In the southwestern part of the catchment, farmland prevails. The lake does not receive pollutants from point sources. Its bottom is diversified, with numerous gullets and underwater hills. Tourists come to Lake Łańskie not only from Poland, but also from abroad, while fish from this lake belonging to the Fisheries Farm are marketed on the local market and beyond. According to the research carried out by the Provincial Inspectorate for Environmental Protection, the level of mercury and its compounds in water in the year 2013 was below the estimate by using the proper standard measurement or standard sample LOQ (limit of quantitation), set at 0.02 μg/L.
After catching the fish, they were taken to the laboratory. On the same day they were weighed and measured. The body weight (± 0.01 g) and total length (± 0.1 cm) of each fish are presented in Table 1. Muscles (without skin) were dissected from the dorsal part, and together with liver, gills and gonads were stored at −30 °C in a refrigerator until analysis. Each sample, prepared from one specimen, was in duplicate. After thawing, the samples were ground and homogenized, then weighed in two parallel repetitions.
Ethical permit: fish were bought at the fish farm and were already dead. According to European and Polish Law, the research done on the tissue of commercially caught fish is free from obtaining permission from the Local Ethical Commission.

2.2. Element Analysis

2.2.1. Mercury

The content of mercury was determined in four organs: muscles, liver, gonads and gills (duplicate samples) using Milestone DMA-80 with a detection limit (LOD) at 0.02 μg/kg. LOD is the lowest value that can be detected with the given analytical procedure and based on statistical significance. The parameters of the method are described in the previous publications [37,42]. The quality of the method was tested using the reference material: BCR CRM 422 (muscles of cod Gadus morhua (L.)) with a certified value of mercury. The recovery rate of Hg was 100.2% (n = 4).

2.2.2. Fat and Fatty Acid Analysis

Approximately 1 g of duplicate samples (±0.0001 g) were dried to a constant weight at 105 °C in glass sample tubes with frits and transferred to weighed beakers. The lipids from the fish muscles (without skin) were hot-extracted in three steps (extraction, rinsing and drying) (E-816HE automatic extractor, BUCHI, Switzerland).
The content of fat (%) was calculated according to the following formula:
x = [(b − a) × 100]/c
where a = weight of flask (g), b = weight of flask with extracted fat (g) and c = weight of samples (g).
For the determination of fatty acids, fat was extracted according to the Folch’s procedure [43]. Sample preparation for the analysis can be found in an earlier publication [30].
The fatty acids of methyl esters of each sample determined the following conditions: capillary column (dimension = 30 m × 0.25 μm, with a 0.32 mm internal diameter, liquid phase StabilwaxR), temperature: flame-ionization detector—250 °C, injector—230 °C, column—190 °C, carrier gas—helium with a flow rate 1.5 mL/min with a flame ionization detector (FID). The apparatus 7890A Agilent Technologies chromatograph (Waldbroon, Germany) was used for analysis, but individual fatty acids were identified by comparing the relative retention time peaks of Supelco’s standards (Supelco, Bellefonte, PA, USA).

2.2.3. Indicators of Environmental Conditions and Fish Quality (FCF, HSI, GSI, MPI and BCF)

The Fulton’s condition factor (FCF) (Table 1) was calculated as described by Łuczyńska et al. [42] and Hamid et al. [44], whereas the value of the hepatosomatic index (HSI) and the gonadosomatic index (GSI) were estimated using the formulae (Table 1) shown in the publication of Łuczyńska et al. [38] and Sadekarpawar and Parikh [45]. The metal pollution index (MPI) was determined using the formulae by Łuczyńska et al. [38], Usero et al. [46,47] and Abdel-Khalek et al. [48] (Table 1), while the bioconcentration factor (BCF) was calculated using the formula proposed by Yarsan and Yipel [5] and Lau et al. [49].

2.2.4. The Lipid Quality Indices

The atherogenicity index (AI) and the thrombogenicity index (TI) (AI and TI, respectively) were calculated as presented by Łuczyńska et al. [37], Ulbricht and Southgate [50], Garaffo et al. [51] and Telahigue et al. [52]. The flesh-lipid quality (FLQ) indicating the percentage correlation between EPA + DHA and the total lipids was determined using the formulae by Łuczyńska et al. [37], Abrami et al. [53] and Senso et al. [54]. The formulae used to calculate the hypercholesterolemic (OFA) and hypocholesterolemic (DFA) fatty acids are presented in the publication of Łuczyńska et al. [37].

2.2.5. Human Health Risk Assessment

Similar to the target hazard quotient (THQ), the estimated daily intake of mercury (EDI) was calculated as described in earlier publications [30,34].

2.3. Statistical Analysis

Significant differences in the content of fatty acids and lipid quality indexes in the muscles of the fish examined were estimated using a one-way analysis of variance (ANOVA) after testing for the homogeneity of variance (Levene’s test) at a significance level of p ≤ 0.05. Similarly, differences in the mean content of mercury between species and organs of the same species were calculated using STATISTICA 12 software (StatSoft, Kraków, Poland). The correlation coefficients between the content of mercury in the organs of fish and their size (body weight and total length) were evaluated using STATISTICA 12 software.

3. Results

3.1. Mercury and Tools for Monitoring Fish and Environmental Conditions (BCF, MPI, FCF, HSI and GSI)

Mercury contents in the organs of perch were significantly higher than in the organs of roach (p ≤ 0.05) (Table 1). The muscles of fish studied contained significantly more mercury than the other organs. The content of mercury decreased in the following order: muscles > liver > gonads ≈ gills (perch) and muscles > liver > gills > gonads (roach) (Figure 2). Regardless of the species, a positive correlation was found between mercury content in the muscles and the fish weight (Table 2), with respective correlation coefficients determined for perch and roach at r = 0.785 (p = 0.012) (Figure 3a) and r = 0.777 (p = 0.008) (Figure 3b), respectively. A positive correlation was also found between levels of mercury in the muscles of perch and the length of this fish (r = 0.760, p = 0.017) (Figure 3c). All parameters studied were higher in perch than roach (Table 1).

3.2. Human Health Risk Assessment

In 2014, the annual fish consumption was 12.3 kg/per capita/year [55]. The estimated daily intake (EDI) of mercury from the 33.698 g portions of fish was 0.124 μg/kg/day (perch) and 0.048 μg/kg/day (roach) (Table 3). The weekly intake of mercury with the 235.89 g portion of perch and roach flesh accounted for 21.73% and 8.31% of the TWI (for inorganic mercury expressed as 4 µg/kg body weight), and for 66.87% and 25.58% of the TWI (for methylmercury expressed as 1.3 μg/kg body weight), respectively. The content of mercury was lower than the maximum acceptable level (0.5 mg/kg) estimated by the Commission Regulation (EC) No 629/2008 of 2 July 2008. The target hazard quotient (THQ) for mercury in the fish examined is shown in Table 3.

3.3. Fatty Acids

Differences between Ʃ SFA (saturated fatty acid), MUFA (monounsaturated fatty acid) and n-3 PUFA (polyunsaturated fatty acid) in the muscles lipids of the fish examined were not statistically significant (p > 0.05) (Table 4). The muscles of roach contained more Ʃ n-6 PUFA (polyunsaturated fatty acid) than the muscle tissue of perch (p ≤ 0.05), but the n-3/n-6 ratio was statistically significantly higher (p ≤ 0.05) in the muscles of perch than in the same tissue of roach. The most abundant SFA in both studied fish was palmitic acid C16:0, whereas oleic acid (C18:1) was the major MUFA group. The differences in the content of palmitic acid between the muscles of perch and roach (20.64% and 20.63%, respectively) were not significant (p > 0.05). The percentage of oleic acid in the muscles of perch was significantly higher (14.48%) than in the muscle tissue of roach (11.17%) (p ≤ 0.05). Arachidonic acid (C20:4 n-6, AA) was the major n-6 polyunsaturated fatty acid, and its higher content was determined in the muscles of roach (10.04%) than perch (7.64%) (p ≤ 0.05). Docosahexaenoic acid (C22:6 n-3, DHA) was the major n-3 polyunsaturated fatty acid, and its contents determined in the muscle tissue of perch and roach (22.78 and 23.81%, respectively) did not differ significantly (p > 0.05)

3.4. Lipid Quality Indexes

A significantly higher index of atherogenicity (AI) characterized the muscles of perch (0.40) than roach (0.35) (p ≤ 0.05) (Table 2). There were no significant differences between the value of the thrombogenicity index (TI), flesh-lipid quality index (FLQ), hypercholesterolemic fatty acids (OFA) and hypocholesterolemic fatty acids (DFA) in the muscles of the fish examined (p > 0.05).

4. Discussion

Kareem et al. [59] found that a higher growth rate of fish and good habitat conditions are indicated by higher HSI values. In contrast, lower HSI values mean adverse environmental effects to fish health, which affects their growth. Therefore, the value of HSI provides valuable information not only about the health of fish, but also about the quality of the aquatic ecosystem. Pieterse [60] has stated that GSI is a biomarker of exposure to toxic fish and that histopathology is a useful tool to assess the degree of contamination. Similarly, Tsoumani et al. [61] have reported that FCF can be used as a good indicator of the quality of water ecosystems inhabited by fish or of the general health of fish populations. Based on the low MPI, it can be concluded that Lake Łańskie is not exposed to direct pollution. As suggested by Sauliutė et al. [3], the higher BCF values indicate more intense bioconcentration of metals in fish. The values of other indicators also show that Lake Łańskie is an aquatic reservoir unpolluted with mercury. According to Kuklina et al. [62], the muscles of perch had a higher mercury content than other fish from drinking water reservoirs (Czech Republic) (perch > pikeperch > rudd > tench > roach > bream). These results are consistent with those found in the present research (Table 1). In turn, predatory fish (salmon trout, pike and perch) were reported to contain more mercury than the benthophages (whitefish and bream) from the European Russian lakes and rivers. In addition, mercury content decreased as follows: salmon trout > pike > perch > whitefish > bream. The same authors found high mercury contents in the liver and muscles (liver ≥ muscles ≥ kidney > gills ≥ skeleton), and stated that liver and muscles may be recommended indicators of mercury pollution of basins (Montenegro [63]). Mercury contents were generally found to increase with trophic levels, because they were the highest (0.093 mg/kg) in high trophic level predatory fish, followed by middle trophic level predatory fish (0.063 mg/kg) and low trophic level fish (0.047 mg/kg), however, the differences were not significant (p > 0.05) [64]. In contrast, Kalisinska et al. [65] found no differences in mercury content between benthophages and phytophages, but showed mercury contents to differ significantly between predators and benthivores. Ðikanović et al. [66] found that the bioaccumulation of metals, including Hg, in organs of fish from West Morava River Basin (Serbia) could be ordered as follows: Prussian carp > northern pike > freshwater bream > European perch > chub > common nase > barbell > roach > European catfish. According to Łuczyńska et al. [67], the concentration of mercury in fish decreased as follows: ide ≈ perch ≈ flounder > rainbow trout > bream ≈ carp (in liver), perch ≈ ide > flounder > bream ≈ rainbow trout > carp (in muscles) and perch ≈ flounder ≈ ide > rainbow trout > bream ≈ carp (in gills) (p ≤ 0.05). The order of mercury accumulation in fish muscles found by Rakocevic et al. [68] was: eel > perch > rudd > carp > roach > bleak, but with no significant differences between the species. These authors reported no significant correlations between mercury content in the muscles of fish studied and their age and size. In turn, a positive correlation between total mercury concentration in the muscles of roach and perch from four lakes in the Olsztyn Lake District (Poland) was found by Łuczyńska et al. [69]. This is in accordance with the data of the present study.
The THQ values were below 1, hence it is known that there is no non-carcinogenic health risk for people by consuming meat obtained from the fish examined (Table 3). According Łuczyńska et al. [37], Sadekarpawar and Parikh [45] and Khemis et al. [58] THQ values in freshwater fish were also below 1. Kimáková et al. [70] showed that the maximum mercury level decreed by the Ministry of Aquaculture of the Slovak Republic and by the European Commission Regulation was exceeded in 50.52% of all fish studied. Large specimens of high trophic level pelagic and demersal species from the Central Adriatic and Tyrrhenian coasts of Italy exceeded the maximum limit appointed by the European Commission, whereas the authors detected a lower content of mercury in low trophic level demersal and pelagic-neritic fish and in young specimens belonging to high trophic level species [71]. In turn, the content of mercury in the muscle tissue of six different fish species from the Danube River (Belgrade) was below the maximum allowable level in the Republic of Serbia [66]. Olmedo et al. [72] found high content of mercury in some predatory fish, which was, however, below the regulatory maximum level set by the EC Regulation. According to Strandberg et al. [73], the consumption of perch from humic lakes exposed humans to greater risks (higher concentrations of mercury), and provided fewer benefits (lower concentrations of EPA + DHA) than consumption of perch from clear lakes. The total contents of EPA and DHA in 100 g of muscle tissue of the fish from the Vistula Lagoon were as follows: eel—2.11 g; herring—0.62 g; bream—0.33 g; roach—0.19 g; perch—0.16 g; and pikeperch—0.14 g (the recommended daily dose for healthy persons is 0.5 g) [74].
The chemical composition of fish (i.e., water, proteins, lipids, vitamins and minerals fatty acids) varies among one species and individual fish, but it also depends on age, sex, environment and season [75]. According to Vasconi et al. [76], planktivorous fish contained the lowest values of n-3 PUFA, but the highest amounts of MUFA (p ≤ 0.05). These authors also found that the carnivorous fish had the highest amounts of SFA and n-3 PUFA (p ≤ 0.05), but the lowest content of MUFA. In turn, Łuczyńska et al. [77] reported that non-predatory fish (bream, vendace and roach) contained lower amount of SFAs than the predatory fish (perch, pike and burbot) (Mazurian Great Lakes, Poland) (p ≤ 0.05). An opposite dependency was observed in the case of total n-3 PUFAs and EPAs (p ≤ 0.05), whereas the amounts of MUFAs, n-6 PUFAs, DHAs and the n-3/n-6 ratio were similar in the two groups of fish (p > 0.05). These results are not consistent with those observed in the perch and roach examined, being representatives of predatory and non-predatory fish, respectively (Table 2). Kainz et al. [78] studied dorsal muscles of the following species: Arctic charr (Salvelinus alpinus L.), pike (Esox lucius L.), perch (Perca fluviatilis L.), brown trout (Salmo trutta L.), roach (Rutilus rutilus L.) and minnow (Phoxinus phoxinus L.) from Lake Lunz, Austria and found that contents of n-3 and n-6 PUFA in these fish decreased with the increasing trophic position, which demonstrated that the bioaccumulation of these essential fatty acids did not increase with the increasing trophic level. In turn, Woźniak et al. [79] showed that the nutritional value (including fatty acids) of fish from lakes of northeastern Poland and fish farms was affected by species-specific traits, environmental conditions and aquaculture techniques.
AI and TI of the flesh of 13 freshwater fish (Czech Republic) ranged from 0.27 to 0.63 and from 0.20 to 0.61, respectively. These results suggest that the flesh of all examined species (except for Nile Tilapia) is of high nutritional quality and affords great benefits to human health [80]. According to De Sousa et al. [81], Nile tilapia from continental aquaculture in Paraiba State (Brazil) can be recommended for human consumption due to low AI and TI indices and hypocholesterolemic/hypercholesterolemic fatty acids ratio (H/H). Similarly, all of the farmed fish species except turbot (Scophthalmus maximus L.) had the recommended levels of the atherogenicity index, thrombogenicity index and hypocholesterolemic to hypercholesterolemic fatty acids ratio, whereas the highest flesh-lipid quality value was observed in the dentex (Dentex dentex L.) [82].

5. Conclusions

Human health is exposed in the case of contact with very harmful mercury. Perch, belonging to the last link in the trophic chain of the Łanskie Lake, due to the higher bioaccumulation capacity of mercury, should be a bioindicator of Łańskie Lake. Fish such as perch accumulated more mercury in their organs than the roach, which occupies the lower level. Although the level of mercury was higher in fish muscles than other organs, it did not exceed the acceptable standards and depended on fish size. Based on the indices that provide information on the quality of aquatic ecosystems, it can be concluded that Łańskie Lake is not exposed to mercury pollution, which is also confirmed by the research of the Provincial Inspectorate for Environmental Protection. A THQ level below 1.00 indicates that these fish are safe from a nutritional point of view, while low values of AI and TI indices and a high DFA indicate that the flesh of these fish is also richer in fatty acids, having the desired dietary effect for humans. The obtained research results indicate that even in the era of globalization, it is possible to find environments free from heavy metals, from which the fish obtained can be safely consumed by humans. At the same time, the examination of indicator fish such as roach and perch clearly indicate the quality of the aquatic environment in which these fish live.

Author Contributions

J.Ł. had the original idea for the study and wrote the manuscript, B.P. and J.Ł. collected and analyzed the data, M.J.Ł. and M.K.-G. conducted the statistical analysis, B.P. contributed in the writing of the section “Analytical methods”. M.J.Ł. contributed in the writing of the section “Results”, D.K. and J.N. contributed to the manuscript revision process—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This study received no external financing.

Conflicts of Interest

The authors declare no conflict of interest regarding the publication of this article.

References

  1. Starmach, K.; Wróbel, S.; Pasternak, K. Hydrobiologia. Limnologia; PWN: Warsaw, Poland, 1976. [Google Scholar]
  2. Sadowska, U. The importance of bioindication in water ecotoxicology. SEeB 2012, 10, 33–52. [Google Scholar] [CrossRef]
  3. Sauliutė, G.; Stankevičiūtė, M.; Svecevičius, G.; Baršiene, J.; Valskienė, R. Assessment of heavy metals bioconcentration factor (BCF) and genotoxicity response induced by metal mixture in Salmo salar tissues. In Proceedings of the Environmental Engineering 10th International Conference, Vilnius, Lithuania, 27–28 April 2017. [Google Scholar] [CrossRef]
  4. Barron, M.G. Bioaccumulation and bioconcentration in aquatic organisms. In Handbook of Ecotoxicology; Hoffman, D.J., Rattner, B.A., Burton, G.A., Jr., Cairns, J., Jr., Eds.; CRC Press Company: Boca Raton, FL, USA, 2003; pp. 877–892. [Google Scholar]
  5. Yarsan, E.; Yipel, M. The Important Terms of Marine Pollution “Biomarkers and Biomonitoring, Bioaccumulation, Bioconcentration, Biomagnification”. J. Mol. Biomark. Diagn. 2013, 1, 1–4. [Google Scholar] [CrossRef]
  6. Mackay, D.; Celsie, A.K.D.; Powell, D.E.; Parnis, J.M. Bioconcentration, bioaccumulation, biomagnification and trophic magnification: A modelling perspective. Environ. Sci. Process. Impacts 2018, 20, 72–85. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Zeitoun, M.M.; Mehana, E.E. Impact of water pollution with heavy metals on fish health: Overview and updates. Glob. Vet. 2014, 12, 219–231. [Google Scholar] [CrossRef]
  8. Lodenius, M. Accumulation and fluxes of mercury in terrestrial and aquatic food chains with special reference to Finland. Eur. J. Environ. Sci. 2012, 2, 77–83. [Google Scholar] [CrossRef] [Green Version]
  9. World Health Organization (WHO). Elemental Mercury and Inorganic Mercury Compounds: Human Health Aspects. Concise International Chemical Assessment Document 50; World Health Organization: Geneva, Switzerland, 2003. [Google Scholar]
  10. Szczerbowski, A.; Kucharczyk, D.; Mamcarz, A.; Łuczyński, M.J.; Targońska, K.; Kujawa, R. Artificial off-season spawning of Eurasian perch Perca fluviatilis L. Arch. Pol. Fish. 2009, 17, 95–98. [Google Scholar] [CrossRef] [Green Version]
  11. Kujawa, R.; Kucharczyk, D.; Mamcarz, A.; Żarski, D.; Targońska, K. Artificial spawning of common tench Tinca tinca (Linnaeus, 1758), obtained from wild and domestic stocks. Aquac. Int. 2011, 19, 513–521. [Google Scholar] [CrossRef] [Green Version]
  12. Kucharczyk, D.; Nowosad, J.; Kujawa, R.; Dietrich, G.; Biegaj, M.; Sikora, M.; Łuczyński, M.J. Comparison of spontaneous and hormone-induced reproduction of burbot (Lota lota L.) under hatchery conditions. Aquaculture 2018, 485, 25–29. [Google Scholar] [CrossRef]
  13. Kucharczyk, D.; Nowosad, J.; Kucharczyk, D.J.; Kupren, K.; Targońska, K.; Wyszomirska, E.; Kujawa, R. Out-of-season artificial reproduction of common dace (Leuciscus leuciscus L.) under controlled conditions. Anim. Reprod. Sci. 2019, 202, 21–25. [Google Scholar] [CrossRef]
  14. Kucharczyk, D.; Nowosad, J.; Wyszomirska, E.; Cejko, B.I.; Arciuch-Rutkowska, M.; Juchno, D.; Boroń, A. Comparison of artificial spawning effectiveness of hCG, CPH and GnRHa in combination with dopamine inhibitors in a wild strain of ide Leuciscus idus (L.) in hatchery conditions. Anim. Reprod. Sci. 2020, 221, 106543. [Google Scholar] [CrossRef] [PubMed]
  15. Sikora, M.; Nowosad, J.; Biegaj, M.; Kucharczyk, D.; Dębowski, M. The possibility of application of agglomerate elastomers (EPP) as media for biological bed in aquaculture. Aquac. Res. 2018, 49, 2988–2994. [Google Scholar] [CrossRef]
  16. Sikora, M.; Nowosad, J.; Kucharczyk, D. Comparison of Different Biofilter Media during Biological Bed Maturation Using Common Carp as a Biogen Donor. Appl. Sci. 2020, 10, 626. [Google Scholar] [CrossRef] [Green Version]
  17. Nowosad, J.; Kucharczyk, D. First report of the occurrence and different types of conjoined twins in common whitefish Coregonus maraena larvae originating from the Baltic Sea. Dis. Aquat. Org. 2019, 132, 163–170. [Google Scholar] [CrossRef] [PubMed]
  18. Nowosad, J.; Kucharczyk, D.; Łuczyńska, J. Changes in mercury concentration in muscles, ovaries and eggs of European eel during maturation under controlled conditions. Ecotoxicol. Environ. Saf. 2018, 148, 857–861. [Google Scholar] [CrossRef]
  19. Nowosad, J.; Sieszputowska, J.; Kucharczyk, D.; Łuczyńska, J.; Sikora, M.; Kujawa, R. Dynamics of mercury content in adult sichel (Pelecus cultratus L.) tissues from the Baltic Sea before and during spawning. Mar. Environ. Res. 2019, 148, 75–80. [Google Scholar] [CrossRef]
  20. Helfrich, L.A.; Neves, R.J. Sustaining America’s aquatic biodiversity—Freshwater fish biodiversity and conservation. VCE Publ. 2009, 420–525, 1–6. [Google Scholar]
  21. Zdrojewicz, Z.; Adamek, M.; Machelski, A.; Wójcik, E. The influence of fatty acids (omega) contained in fish on the man organism. Med. Rodzinna. 2015, 3, 137–143. [Google Scholar]
  22. Rustan, A.C.; Drevon, C.A. Fatty Acids: Structures and Properties. eLS 2005, 1–7. [Google Scholar] [CrossRef]
  23. Lucio, G.C.; Vittorio, F. Joint FAO/WHO Expert Consultation on the Risks and Benefits of Fish Consumption; FAO: Rome, Italy, 2010; p. 63. [Google Scholar]
  24. Strungaru, S.-A.; Nicoarã, M.; Rãu, M.A.; Plãvan, G.; Micu, D. Do you like to eat fish? An overview of the benefits of fish consumption and risk of mercury poisoning. Biol. Anim. 2015, 61, 117–123. [Google Scholar]
  25. Lunn, J.; Theobald, H.E. The health effects of dietary unsaturated fatty acids. Nutr. Bull. 2006, 31, 178–224. [Google Scholar] [CrossRef]
  26. Djazayery, A.; Jazayery, S. ω-3 fatty acids in physical and mental health and disease. In Wild-Type Food in Health Promotion and Disease Prevention; De Meester, F., Watson, R.R., Eds.; Humana Press Inc.: Totowa, NJ, USA, 2008; pp. 309–321. [Google Scholar]
  27. Harris, W.S. The omega-3 index as a risk factor for coronary heart disease. Am. J. Clin. Nutr. 2008, 87, 1997S–2002S. [Google Scholar] [CrossRef]
  28. Das, U.N. Biological significance of essential fatty acids. J. Assoc. Phys. India 2006, 54, 309–319. [Google Scholar]
  29. Lorente-Cebrián, S.; Costa, A.G.V.; Navas-Carretero, S.; Zabala, M.; Martínez, J.A.; Moreno-Aliaga, M.J. Role of omega-3 fatty acids in obesity, metabolic syndrome, and cardiovascular diseases: A review of the evidence. J. Physiol. Biochem. 2013, 69, 633–651. [Google Scholar] [CrossRef] [PubMed]
  30. Ristić-Medić, D.; Vučić, V.; Takić, M.; Karadžić, I.; Glibetić, M. Polyunsaturated fatty acids in health and disease. J. Serb. Chem. Soc. 2013, 78, 1269–1289. [Google Scholar] [CrossRef]
  31. Calder, P.C. Very long chain omega-3 (n-3) fatty acids and human health. Eur. J. Lipid Sci. Technol. 2014, 116, 1280–1300. [Google Scholar] [CrossRef]
  32. Kim, K.-B.; Nam, Y.A.; Kim, H.S.; Hayes, A.W.; Lee, B.-M. α-Linolenic acid: Nutraceutical, pharmacological and toxicological evaluation. Food Chem. Toxicol. 2014, 70, 163–178. [Google Scholar] [CrossRef]
  33. Bowen, K.J.; Harris, W.S.; Kris-Etherton, P.M. Omega-3 Fatty Acids and Cardiovascular Disease: Are There Benefits? Curr. Treat. Options Cardiovasc. Med. 2016, 18, 69. [Google Scholar] [CrossRef] [Green Version]
  34. Yang, Z.-H.; Emma-Okon, B.; Remaley, A.T. Dietary marine-derived long-chain monounsaturated fatty acids and cardiovascular disease risk: A mini review. Lipids Health Dis. 2016, 15, 1–9. [Google Scholar] [CrossRef] [Green Version]
  35. Figuiredo, P.S.; Inada, A.C.; Marcelino, G.; Lopes Cardozo, C.M.; de Cássia Freitas, K.; de Cássia Avellaneda Guimarães, R.; de Castro, A.P.; do Nascimento, V.A.; Hiane, P.A. Fatty Acids Consumption: The Role Metabolic Aspects Involved in Obesity and Its Associated Disorders. Nutrients 2017, 9, 1158. [Google Scholar] [CrossRef] [Green Version]
  36. Olgunoglu, I.A. Review on omega-3 (n-3) fatty acids in fish and seafood. J. Biol. Agric. Healthc. 2017, 7, 37–45. [Google Scholar]
  37. Łuczyńska, J.; Paszczyk, B.; Nowosad, J.; Łuczyński, M.J. Mercury, Fatty Acids Content and Lipid Quality Indexes in Muscles of Freshwater and Marine Fish on the Polish Market. Risk Assessment of Fish Consumption. Int. J. Environ. Res. Public Health 2017, 14, 1120. [Google Scholar] [CrossRef] [PubMed]
  38. Łuczyńska, J.; Paszczyk, B.; Łuczyński, M.J. Fish as a bioindicator of heavy metals pollution in aquatic ecosystem of Pluszne Lake, Poland, and risk assessment for consumer’s health. Ecotoxicol. Environ. Saf. 2018, 153, 60–67. [Google Scholar] [CrossRef]
  39. Łuczyńska, J.; Paszczyk, B. Health Risk Assessment of Heavy Metals and Lipid Quality Indexes in Freshwater Fish from Lakes of Warmia and Mazury Region, Poland. Int. J. Environ. Res. Public Health 2019, 16, 3780. [Google Scholar] [CrossRef] [Green Version]
  40. Domingo, J.L. Omega-3 fatty acids and the benefits of fish consumption: Is all that glitters gold? Environ. Int. 2007, 33, 993–998. [Google Scholar] [CrossRef] [PubMed]
  41. Food and Agriculture Organization (FAO). Food and Nutrition Paper. Fats and Fatty Acids in Human Nutrition; Report of an Expert Consultation; FAO: Rome, Italy, 2010. [Google Scholar]
  42. Łuczyńska, J.; Łuczyński, M.J.; Paszczyk, B.; Tońska, E. Concentration of mercury in muscles of predatory and non-predatory fish from lake Pluszne (Poland). J. Vet. Res. 2016, 60, 43–47. [Google Scholar] [CrossRef] [Green Version]
  43. Christie, W.W. The isolation of lipids from tissues. Recommended Procedures. Chloroform-methanol (2:1, v/v) extraction and “Folch” wash. In Lipid Analysis. Isolation, Separation, Identification and Structural Analysis of Lipids; Christie, W.W., Ed.; Pergamon Press: Oxford, UK, 1973; pp. 39–40. [Google Scholar]
  44. Hamid, M.A.; Mansor, M.; Nor, S.A.M. Length-weight Relationship and Condition Factor of Fish Populations in Temengor Reservoir: Indication of Environmental Health. Sains Malays. 2015, 44, 61–66. [Google Scholar] [CrossRef]
  45. Sadekarpawar, S.; Parikh, P. Gonadosomatic and hepatosomatic indices of freshwater fish Oreochromis mossambicus in response to a plant nutrient. World J. Zool. 2013, 8, 110–118. [Google Scholar] [CrossRef]
  46. Usero, J.; Gonzalez-Regalado, E.G.; Gracia, I. Trace metals in bivalve molluscs Chamelea gallina from the Atlantic coast of southern Spain. Mar. Pollut. Bull. 1996, 32, 305–310. [Google Scholar] [CrossRef]
  47. Usero, J.; Regalado, E.G.; Gracia, I. Trace metals in bivalve molluscs Ruditapes decussatus and Ruditapes philippinarum from the Atlantic coast of southern Spain. Environ. Int. 1997, 23, 291–298. [Google Scholar] [CrossRef]
  48. Abdel-Khalek, A.A.; Elhaddad, E.; Mamdouh, S.; Saed Marie, M.-A. Assessment of metal pollution around Sabal Drainage in River Nile and its impacts on bioaccumulation level, metals correlation and human risk hazard using Oreochromis niloticus as a bioindicator. Turk. J. Fish. Aquat. Sci. 2016, 16, 227–239. [Google Scholar] [CrossRef]
  49. Lau, S.; Mohamed, M.; Yen, A.T.C.; Su’Ut, S. Accumulation of heavy metals in freshwater molluscs. Sci. Total Environ. 1998, 214, 113–121. [Google Scholar] [CrossRef]
  50. Ulbricht, T.; Southgate, D. Coronary heart disease: Seven dietary factors. Lancet 1991, 338, 985–992. [Google Scholar] [CrossRef]
  51. Garaffo, M.A.; Vassallo-Agius, R.; Nengas, Y.; Lembo, E.; Rando, R.; Maisano, R.; Dugo, G.; Giuffrida, D. Fatty Acids Profile, Atherogenic (IA) and Thrombogenic (IT) Health Lipid Indices, of Raw Roe of Blue Fin Tuna (Thunnus thynnus L.) and Their Salted Product “Bottarga”. Food Nutr. Sci. 2011, 2, 736–743. [Google Scholar] [CrossRef] [Green Version]
  52. Telahigue, K.; Hajji, T.; Rabeh, I.; El Cafsi, M. The changes of fatty acid composition in sun dried, oven dried and frozen hake (Merluccius merluccius) and sardinella (Sardinella aurita). Afr. J. Biochem. Res. 2013, 7, 158–164. [Google Scholar] [CrossRef]
  53. Abrami, G.; Natiello, F.; Bronzi, P.; McKenzie, D.; Bolis, L.; Agradi, E. A comparison of highly unsaturated fatty acid levels in wild and farmed eels (Anguilla Anguilla). Comp. Biochem. Phys 1992, 101, 79–81. [Google Scholar] [CrossRef]
  54. Senso, L.; Suárez, M.; Ruiz-Cara, T.; García-Gallego, M. On the possible effects of harvesting season and chilled storage on the fatty acid profile of the fillet of farmed gilthead sea bream (Sparus aurata). Food Chem. 2007, 101, 298–307. [Google Scholar] [CrossRef]
  55. Statistical Yearbook of Agriculture. Food Economy, Consumption. 2015. Available online: http://stat.gov.pl/en/topics/statistical-yearbooks/statistical-yearbooks/statistical-yearbook-of-agriculture-2015,6,10.html (accessed on 6 October 2020).
  56. United States Environmental Protection Agency (US EPA). Regional Screening Level (RSL) Summary Table; EPA Headquarters: Washington, DC, USA, 2017.
  57. European Food Safety Authority (EFSA) Panel on Contaminants in the Food Chain (CONTAM). Scientific Opinion on the risk for public health related to the presence of mercury and methylmercury in food. EFSA J. 2012, 10, 2985. [Google Scholar] [CrossRef]
  58. Khemis, I.B.; Aridh, N.B.; Hamza, N.; M’Hetli, M.; Sadok, S. Heavy metals and minerals contents in pikeperch (Sander lucioperca), carp (Cyprinus carpio) and flathead grey mullet (Mugil cephalus) from Sidi Salem Reservoir (Tunisia): Health risk assessment related to fish consumption. Environ. Sci. Pollut. Res. 2017, 24, 19494–19507. [Google Scholar] [CrossRef]
  59. Kareem, O.K.; Ajani, E.K.; Orisasona, O.; Olanrewaju, A.N. The Sex Ratio, Gonadosomatic Index, Diet Composition and Fecundity of African Pike, Hepsetus odoe (Bloch, 1794) in Eleyele Lake, Nigeria. J. Fish. Livest. Prod. 2015, 3, 1–4. [Google Scholar] [CrossRef]
  60. Pieterse, G.N. Histopathological Changes in the Testis of Oreochromis Mossambicus (Cichlidae) as a Biomarker of Heavy Metal Pollution. Ph.D. Thesis, Faculty of Science, Rand Afrikaans University, Johannesburg, South Africa, 2004. [Google Scholar]
  61. Tsoumani, M.; Liasko, R.; Moutsaki, P.; Kagalou, I.; Leonardos, I. Length-weight relationships of an invasive cyprinid fish (Carassius gibelio) from 12 Greek lakes in relation to their trophic states. J. Appl. Ichthyol. 2006, 22, 281–284. [Google Scholar] [CrossRef]
  62. Kuklina, I.; Kouba, A.; Buřič, M.; Horká, I.; Ďuriš, Z.; Kozák, P. Accumulation of Heavy Metals in Crayfish and Fish from Selected Czech Reservoirs. BioMed Res. Int. 2014, 2014, 306103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Moiseenko, T.I.; Gashkina, N.A. Bioaccumulation of mercury in fish as indicator of water pollution. Geochem. Int. 2016, 54, 485–493. [Google Scholar] [CrossRef]
  64. Voegborlo, R.B.; Adimado, A.A. Total Mercury Distribution in Different Fish Species Representing Different Trophic levels from the Atlantic Coast of Ghana. J. Sci. Technol. 2010, 30, 109. [Google Scholar] [CrossRef]
  65. Kalisinska, E.; Lanocha-Arendarczyk, N.; Kosik-Bogacka, D.; Budis, H.; Pilarczyk, B.; Tomza-Marciniak, A.; Podlasinska, J.; Cieslik, L.; Popiolek, M.; Pirog, A.; et al. Muscle mercury and selenium in fishes and semiaquatic mammals from a selenium-deficient area. Ecotoxicol. Environ. Saf. 2017, 136, 24–30. [Google Scholar] [CrossRef] [PubMed]
  66. Djikanovic, V.; Skorić, S.; Gacic, Z. Concentrations of metals and trace elements in different tissues of nine fish species from the Medjuvrsje reservoir (West Morava River Basin, Serbia). Arch. Biol. Sci. 2016, 68, 811–819. [Google Scholar] [CrossRef] [Green Version]
  67. Łuczyńska, J.; Łuczyński, M.J.; Paszczyk, B. Assessment of mercury in muscles, liver and gills of marine and freshwater fish. J. Elem. 2016, 21, 113–129. [Google Scholar] [CrossRef]
  68. Rakocevic, J.; Sukovic, D.; Maric, D. Distribution and relationships of eleven trace elements in muscle of six fish species from Skadar Lake (Montenegro). Turk. J. Fish. Aquat. Sci. 2018, 18, 647–657. [Google Scholar] [CrossRef]
  69. Łuczyńska, J. The influence of weight and length on the mercury content in the muscle tissue of fish from four lakes in the Olsztyn Lake District (Poland). Arch. Pol. Fish. 2005, 13, 51–61. [Google Scholar]
  70. Kimakova, T.; Kuzmová, L.; Nevolná, Z.; Bencko, V. Fish and fish products as risk factors of mercury exposure. Ann. Agric. Environ. Med. 2018, 1–6. [Google Scholar] [CrossRef] [Green Version]
  71. Di Lena, G.; Casini, I.; Caproni, R.; Fusari, A.; Orban, E. Total mercury levels in commercial fish species from Italian fishery and aquaculture. Food Addit. Contam. Part B 2017, 1–18. [Google Scholar] [CrossRef]
  72. Olmedo, P.; Pla, A.; Hernández, A.F.; Barbier, F.; Ayouni, L.; Gil, F. Determination of toxic elements (mercury, cadmium, lead, tin and arsenic) in fish and shellfish samples. Risk assessment for the consumers. Environ. Int. 2013, 59, 63–72. [Google Scholar] [CrossRef]
  73. Strandberg, U.; Palviainen, M.; Eronen, A.; Piirainen, S.; Laurén, A.; Akkanen, J.; Kankaala, P. Spatial variability of mercury and polyunsaturated fatty acids in the European perch (Perca fluviatilis)—Implications for risk-benefit analyses of fish consumption. Environ. Pollut. 2016, 219, 305–314. [Google Scholar] [CrossRef] [PubMed]
  74. Polak-Juszczak, L.; Komar-Szymczak, K. Fatty acid profiles and fat contents of commercially important fish from Vistula Lagoon. Pol. J. Food Nutr. Sci. 2009, 59, 225–229. [Google Scholar]
  75. Sándor, Z.; Papp, Z.G.; Csengeri, I.; Jeney, Z. Fish meat quality and safety. Tehnol. Mesa. 2011, 52, 97–105. [Google Scholar]
  76. Vasconi, M.; Caprino, F.; Bellagamba, F.; Busetto, M.L.; Bernardi, C.; Puzzi, C.; Moretti, V.M. Fatty Acid Composition of Freshwater Wild Fish in Subalpine Lakes: A Comparative Study. Lipids 2015, 50, 283–302. [Google Scholar] [CrossRef]
  77. Łuczyńska, J.; Borejszo, Z.; Łuczyński, M.J. The Composition of Fatty Acids in Muscles of Six Freshwater Fish Species from the Mazurian Great Lakes (Northeastern Poland). Arch. Pol. Fish. 2008, 16, 167–178. [Google Scholar] [CrossRef] [Green Version]
  78. Kainz, M.J.; Hager, H.H.; Rasconi, S.; Kahilainen, K.K.; Amundsen, P.-A.; Hayden, B. Polyunsaturated fatty acids in fishes increase with total lipids irrespective of feeding sources and trophic position. Ecosphere 2017, 8, 1–13. [Google Scholar] [CrossRef]
  79. Woźniak, M.; Poczyczyński, P.; Kozłowski, K. The nutritional value of selected species of fish from lake and fish farm of north-eastern Poland. Pol. J. Nat. Sci. 2013, 28, 295–304. [Google Scholar]
  80. Linhartová, Z.; Krejsa, J.; Zajic, T.; Masilko, J.; Sampels, S.; Mraz, J. Proximate and fatty acid composition of 13 important freshwater fish species in central Europe. Aquac. Int. 2018, 26, 695–711. [Google Scholar] [CrossRef]
  81. Sousa, Á.B.B.D.; Santos Júnior, O.D.O.; Visentainer, J.V.; De Almeida, N.M. Total lipid nutritional quality of the adipose tissue from the orbital cavity in Nile tilapia from continental aquaculture. Acta Sci. Anim. Sci. 2017, 39, 335. [Google Scholar] [CrossRef] [Green Version]
  82. Pleadin, J.; Lešić, T.; Krešić, G.; Barić, R.; Bogdanović, T.; Oraić, D.; Vulić, A.; Legac, A.; Zrnčić, S. Nutritional quality of different fish species farmed in the Adriatic Sea. Ital. J. Food Sci. 2017, 29, 537–549. [Google Scholar]
Figure 1. Study area was located in northeastern Poland, near the city Olsztyn (geographical coordinates: 53°58′60″ N, 20°48′08″ E).
Figure 1. Study area was located in northeastern Poland, near the city Olsztyn (geographical coordinates: 53°58′60″ N, 20°48′08″ E).
Ijerph 17 07595 g001
Figure 2. Interspecific differences (Mean ± SD) in the content of mercury in the organs of the same fish species; a, b, c and d, significant difference (p ≤ 0.05). The same letter indicates the absence of significant differences between organs of the same fish studied.
Figure 2. Interspecific differences (Mean ± SD) in the content of mercury in the organs of the same fish species; a, b, c and d, significant difference (p ≤ 0.05). The same letter indicates the absence of significant differences between organs of the same fish studied.
Ijerph 17 07595 g002
Figure 3. Relationship between the content of mercury in muscles and the weight and body length of the fish, (a) perch, (b) roach and (c) perch.
Figure 3. Relationship between the content of mercury in muscles and the weight and body length of the fish, (a) perch, (b) roach and (c) perch.
Ijerph 17 07595 g003aIjerph 17 07595 g003b
Table 1. Biometric parameters, BCF and differences between the content of mercury in the same organs of fish examined (mg/kg wet weight).
Table 1. Biometric parameters, BCF and differences between the content of mercury in the same organs of fish examined (mg/kg wet weight).
Perch (Perca Fluviatilis L.) (n = 9)Roach (Rutilus Rutilus L.) (n = 10)
Weight (g)236.22 ± 81.69207.20 ± 38.17
Length (cm)25.66 ± 2.3626.05 ± 1.66
FCF1.337 ± 0.168 a1.165 ± 0.105 b
HSI1.497 ± 0.280 a0.957 ± 0.514 b
GSI4.399 ± 6.554 a0.963 ± 0.508 b
MPI0.068 ± 0.021 a0.027 ± 0.005 b
Mean ± SD
Muscles0.221 ± 0.081 a0.085 ± 0.019 b
Liver0.100 ± 0.047 a0.031 ± 0.008 b
Gonads0.034 ± 0.016 a0.009 ± 0.002 b
Gills0034 ± 0.010 a0.023 ± 0.008 b
BCF
Muscles>11,056.1 ± 4036.3 a>4229.5 ± 954.1 b
Liver>4976.4 ± 2352.4 a>1550.5 ± 389.3 b
Gonads>1676.7 ± 787.5 a>471.0 ± 96.6 b
Gills>1678.9 ± 499.3 a>1154.0 ± 393.7 b
n, number of fish; SD, standard deviation; Fulton’s condition factor (FCF); hepatosomatic index (HSI); gonadosomatic index (GSI); metal pollution index (MPI); bioconcentration factor (BCF); a and b, significant difference (p < 0.05). The same letter indicates the absence of significant differences between perch and roach.
Table 2. Linear correlation coefficients (r) between mercury content in the organs of perch and roach and body weight, total length or Fulton’s condition factor (FCF).
Table 2. Linear correlation coefficients (r) between mercury content in the organs of perch and roach and body weight, total length or Fulton’s condition factor (FCF).
WeightLengthMusclesLiverGonadsGillsFCF
Perch (Perca fluviatilis L.) (n = 9)
Weight
Length0.978
p = 0.000
Muscles0.7850.760
p = 0.012p = 0.017
Liver0.4840.5450.408
p = 0.187p = 0.129p = 0.276
Gonads0.0100.0360.2450.485
p = 0.979p = 0.927p = 0.526p = 0.186
Gills−0.202−0.140−0.1240.4100.788
p = 0.602p = 0.719p = 0.751p = 0.273p = 0.012
FCF0.9190.8350.6950.3690.024−0.184
p = 0.000p = 0.005p = 0.038p = 0.329p = 0.951p = 0.635
Roach (Rutilus rutilus L.) (n = 10)
Weight
Length0.847
p = 0.002
Muscles0.7770.448
p = 0.008p = 0.194
Liver0.5510.4700.415
p = 0.099p = 0.170p = 0.232
Gonads0.4970.6200.4430.567
p = 0.144p = 0.056p = 0.200p = 0.087
Gills0.4690.4980.603−0.1490.404
p = 0.172p = 0.143p = 0.065p = 0.681p = 0.246
FCF0.291−0.2590.6160.181−0.151−0.048
p = 0.415p = 0.470p = 0.058p = 0.617p = 0.677p = 0.896
n, number of fish; p, significance level.
Table 3. The hazard quotient calculated for mercury content in the muscle tissue of the fish examined.
Table 3. The hazard quotient calculated for mercury content in the muscle tissue of the fish examined.
EDITWI%TWI * %TWI **THQReferences
RfD
(mg/kg/day)
3 × 10−4[56]
TWI (for inorganic mercury)4[57]
TWI (for methylmercury)1.3
Perca fluviatilis L. (n = 9)0.1240.86921.7366.8710.414This study
Rutilus rutilus L. (n = 10)0.0480.3338.3125.5820.158This study
Rutilus rutilus L. (n = 10)0.0400.2807.0021.500.135[45]
Perca fluviatilis L. (n = 10)0.0910.63715.9249.000.303[37]
Abramis brama L. (n = 6)0.00860.0601.504.6110.029
Perca fluviatilis L. (n = 5)0.07620.53413.3441.0560.254
Leuciscus idus L. (n = 6)0.06040.42310.5732.5270.201
Cyprinus carpio L. (n = 5)0.00430.0240.601.8450.011
Oncorhynchus mykiss Walb.
(n = 6)
0.00810.0571.424.3630.027
Sander lucioperca L. (n = 9) 4.97 × 10−5[58]
Cyprinus carpio L. (n = 9) 1.17 × 10−5
n, number of fish; RfD, oral reference dose (mg/kg/day); EDI is the estimated daily intake (μg/kg body weight/day); THQ, target hazard quotient; TWI = EDI × 7, tolerable weekly intake (µg/kg body weight). * TWI = tolerable weekly intake for inorganic mercury expressed as mercury (4 µg/kg body weight), ** TWI for methylmercury expressed as mercury (1.3 μg/kg body weight).
Table 4. Fatty acid contents (% of total fatty acids) and index of AI and TI in the muscles lipids of the studied perch and roach (Mean ± SD).
Table 4. Fatty acid contents (% of total fatty acids) and index of AI and TI in the muscles lipids of the studied perch and roach (Mean ± SD).
Fatty AcidSystematic NameTrivial NamePerch
(Perca fluviatilis L.) (n = 9)
Roach
(Rutilus rutilus L.) (n = 10)
Fat (%) 0.88 ± 0.560.72 ± 0.26
C12:0dodecanoiclauric0.11 ± 0.02 a0.11 ± 0.02 a
C14:0tetradecanoicmyristic1.94 ± 0.55 a1.11 ± 0.37 b
C16:0hexadecanoicpalmitic20.64 ± 0.70 a20.63 ± 1.43 a
C18:0octadecanoicstearic5.21 ± 0.61 b5.79 ± 0.54 a
C18:1octadecenoicoleic14.48 ± 1.44 a11.17 ± 2.78 b
C18:2(n-6) LAcis, cis-9,12-octadecadienoiclinoleic2.95 ± 0.57 a2.35 ± 0.79 a
C20:4(n-6) AAall cis-5,8,11,14-eicosatetraenoicarachidonic7.64 ± 1.16 b10.04 ± 1.65 a
C18:3(n-3) ALAall cis-9,12,15-octadecatrienoicα-linolenic 1.93 ± 0.67 a1.11 ± 0.68 b
C20:5(n-3) EPAall cis-5,8,11,14,17-eicosapentaenoiceicosapentaenoic7.11 ± 0.46 a6.11 ± 0.55 b
C22:5(n-3) DPAall cis-7,10,13,16,19-docosapentaenoicdocosapentaenoic2.72 ± 0.34 a2.83 ± 0.21 a
C22:6(n-3) DHAall cis-4,7,10,13,16,19-docosahexaenoicdocosahexaenoic22.78 ± 4.4 a23.81 ± 4.27 a
Ʃ SFA 28.93 ± 0.91 a28.72 ± 1.56 a
Ʃ MUFA 21.68 ± 3.38 a17.90 ± 5.28 a
Ʃ n-6 PUFA 13.08 ± 1.47 b17.95 ± 1.85 a
Ʃ n-3 PUFA 36.31 ± 3.86 a35.43 ± 3.35 a
Ʃ PUFA 49.39 ± 3.30 b53.38 ± 4.36 a
Ʃ UFA 71.07 ± 0.91 a71.28 ± 1.56 a
Ʃ n-3 HUFA 33.64 ± 4.46 a34.05 ± 4.03 a
n-3/n-6 2.82 ± 0.48 a1.99 ± 0.24 b
AI 0.40 ± 1.70 a0.35 ± 0.02 b
TI 0.22 ± 0.02 a0.22 ± 0.02 a
FLQ 29.89 ± 4.25 a29.92 ± 4.14 a
OFA 22.68.41 a21.86 ± 1.82 a
DFA 76.27 ± 0.50 a77.07 ± 1.27 a
n, number of fish; SD, standard Deviation; a and b, significant difference (p ≤ 0.05). The same letter indicates the absence of significant differences between perch and roach. Ʃ SFA (saturated fatty acid) contains C12:0, C14:0, C15:0, C16:0, C17:0, C18:0 and C20:0; Ʃ MUFA (monounsaturated fatty acid) contains C14:1, C16:1, C17:1, C18:1, C20:1(n-7), C20:1(n-9) and C20:1(n-11); Ʃ n-6 PUFA (polyunsaturated fatty acid) contains C18:2, C18:3γ-lin, C20:2, C20:3, C20:4 and C22:5; Ʃ n-3 PUFA (polyunsaturated fatty acid) contains C18:3, C18:4, C20:3, C20:4, C20:5 EPA, C22:5 DPA and C22:6 DHA; Ʃ n-3 HUFA (highly unsaturated fatty acid) contains C20:3, C20:4, C20:5 EPA, C22:5 DPA and C22:6 DHA; AI, index of atherogenicity; TI, index of thrombogenicity; FLQ, flesh-lipid quality; OFA, hypercholesterolemic fatty acids; DFA, hypocholesterolemic fatty acids.
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Łuczyńska, J.; Paszczyk, B.; Łuczyński, M.J.; Kowalska-Góralska, M.; Nowosad, J.; Kucharczyk, D. Using Rutilus rutilus (L.) and Perca fluviatilis (L.) as Bioindicators of the Environmental Condition and Human Health: Lake Łańskie, Poland. Int. J. Environ. Res. Public Health 2020, 17, 7595. https://doi.org/10.3390/ijerph17207595

AMA Style

Łuczyńska J, Paszczyk B, Łuczyński MJ, Kowalska-Góralska M, Nowosad J, Kucharczyk D. Using Rutilus rutilus (L.) and Perca fluviatilis (L.) as Bioindicators of the Environmental Condition and Human Health: Lake Łańskie, Poland. International Journal of Environmental Research and Public Health. 2020; 17(20):7595. https://doi.org/10.3390/ijerph17207595

Chicago/Turabian Style

Łuczyńska, Joanna, Beata Paszczyk, Marek Jan Łuczyński, Monika Kowalska-Góralska, Joanna Nowosad, and Dariusz Kucharczyk. 2020. "Using Rutilus rutilus (L.) and Perca fluviatilis (L.) as Bioindicators of the Environmental Condition and Human Health: Lake Łańskie, Poland" International Journal of Environmental Research and Public Health 17, no. 20: 7595. https://doi.org/10.3390/ijerph17207595

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