Increasing environmental pollution in the 21st century threatens not only domestic (land and air) areas, but also aquatic environments. Pollutant levels in aquatic environments, particularly in the form of heavy metals, and their negative effects on aquatic organisms have been the research topic of numerous analyses across many living species. To identify and demonstrate the pollutants in the aquatic environment, bioindicators are used; these are organisms with qualities that allow the quality of a given environment to be determined. For instance, bivalves and gastropods from the mollusk group are frequently used to biologically monitor heavy metal pollution in the marine environment (Conti & Cecchetti 2003; Boudouresque 2004). Gastropods can absorb metals by swallowing, feeding, or absorbing water, and they can accumulate heavy metals in their tissues at a very high rate (Phillips 1977; Koide et al. 1982; Szefer 1986).
Limpets are used in a traditional shellfish dish that is still widely consumed in some regions, such as the Azores (Portugal) or the Canary Islands (Spain) (Pérez et al. 2019). In Turkey,
Therefore, limpets are one of the most important species to be investigated in Turkey. While the studies on the meat yield, distribution, and morphometric, taxonomic, and biological parameters of
Provisional tolerable weekly intake (PTWI) defines the amount of a substance that can be ingested each week without the risk of any adverse health effects during a person's lifetime (FAO/WHO 2004). The daily and weekly consumption rates and carcinogenic risk values were also calculated to determine the possible effects on human health. The data set was compared with the international consumable limits (THQ, TTHQ, and CR values) (TFC 2008; EU 2008; FDA 2001). In addition, the results were evaluated by comparing them with previous studies conducted in other coastal environments.
Izmit Bay (on the Marmara Sea) was the study area selected from Yalova Province. It is a fisherman's shelter located in the city center by fishing vessels, particularly in the first months of the fishing season (September, October, and November). The Samanlı Stream, along which tourism, irrigated agriculture, and industry are important elements of the local economy, also connects to the sea. Besides thermal resources, industrial plants producing chemicals, energy, acrylic fiber, textiles, ships, paper cleaning products, packaging, plastic, automotive parts, marble, and frozen food are also part of the local economy. These areas are exposed to different sources of pollution, such as domestic drainage, tourism, and agricultural wastewater (YESR 2018). To examine the spatial trends of the region and to compare the different heavy metal concentrations caused by pollution, monthly samples were taken between April and November 2009 from the zone of Samanlıdere fishermen's shelter, shown in Figure 1. In the coastal rocky zone, 20 specimens of
Study area
Digestion processes for heavy metal analysis were performed according to Bernhard (1976) and Yap et al. (2004). The
All the statistical analysis was performed using the statistical package SPSS (version 24; SPSS, Chicago, IL); the statistical significance was set at a
In this study, estimated daily intake (EDI) values for each element under study were calculated according to Copat et al. (2013) in order to assess the human health risks from carcinogenic and non-carcinogenic metals associated with mollusk consumption. Estimated weekly intake (EWI) values were also found by multiplying EDI by 7. No data are available on the daily consumption of mollusks. A normal portion of seafood is 0.160 kg (Afonso et al. 2015). Assuming that only one portion is eaten per week, the calculated daily consumption is 0.0228 kg (Gedik & Eryaşar 2020); the EDI values were calculated assuming a 70-kg adult consumes 0.0228 kg of
The physicochemical parameters measured in the seawater and the average values of heavy metals determined in
The physicochemical variables at the sampling stations from the Samanlıdere Fisher Shelter, Yalova
Months | Temperature (°C) | DO (mg l−1) | pH | Salinity (PSU) |
---|---|---|---|---|
April | 15 | 11.21 | 8.31 | 22 |
May | 21.1 | 8.33 | 22 | |
June | 23.8 | 9.85 | 8.33 | 22 |
July | 23.1 | 8.69 | 8.27 | 24 |
August | 8.97 | 8.34 | 23 | |
September | 22.5 | 9.32 | 24 | |
October | 19.2 | 8.42 | 8.41 | 26 |
November | 18.7 | 8.32 | 8.33 |
Heavy metal concentrations in
Months | Cd | Cu | Pb | Ni | Zn | Fe |
---|---|---|---|---|---|---|
April | 2.60 ± 0.008a | 9.36 ± 0.09ae | 1.02 ± 0.016a | 102.0 ± 0.37a | 58.25 ± 0.59a | 1611.00 ± 19.86a |
May | 2.31 ± 0.026b | 9.03 ± 0.04b | 0.86 ± 0.016bce | 74.75 ± 0.32bf | 60.76 ± 0.43b | 1415.00 ± 3.61bd |
June | 3.27 ± 0.028c | 11.44 ± 0.42cd | 0.83 ± 0.005c | 83.65 ± 0.20cd | 66.22 ± 0.84cd | 1337.33 ± 9.53c |
July | 2.55 ± 0.009d | 10.87 ± 0.49d | 0.74 ± 0.009d | 82.81 ± 0.66d | 67.33 ± 0.29d | 1436.33 ± 22.73d |
August | 2.20 ± 0.008eh | 9.22 ± 0.01e | 0.88 ± 0.013ef | 47.59 ± 0.29ef | 80.86 ± 0.56e | 1365.33 ± 4.18e |
September | 2.01 ± 0.005f | 6.33 ± 0.05f | 0.93 ± 0.019f | 46.63 ± 0.29f | 64.35 ± 0.26f | 1120.67 ± 4.26fh |
October | ||||||
November | 2.21 ± 0.006h | 2.45 ± 0.02h | 1.59 ± 0.035h | 16.31 ± 0.02h | 21.12 ± 0.09h | 1134.00 ± 14.00h |
p < 0.05
There has been a significant increase in the regional population in Yalova Province due to increasing industrialization and immigration. According to the YESR (2018) report, the sources of pollution in Yalova are missing or insufficient sewerage, domestic waste water in settlements, waste water from large industrial plants, pesticides, and chemical fertilizers. The region's Samanlı Stream is also one of the main factors in transferring land-based inputs to the sea. In addition, due to heavy ship traffic, it is thought that the shipyards located east and north of the sampling area, maintenance and repair work, and discharged bilge waters may increase heavy metal exposure. Moreover, Yalova Province, located in the Gulf of Izmit in the Sea of Marmara, may also be affected by the existing sources of pollution in the Sea of Marmara. Likewise, there are various reasons for heavy metal pollution in the Sea of Marmara. The main ones are industrial pollution, solid waste, and port activities. The province with the most industrial activity is Kocaeli, which has more than 1,000 industrial sites representing various sectors. Sectors such as oil refining contribute more than 30% of the fuel usage in Turkey through petrochemical complexes, hazardous and medical waste incineration plants, LPG filling facilities, textile production, tire production, machinery, mining, metals, food, automotive production and services, paper, chemistry, wood, tanning, coal, etc. (Pekey et al. 2004; Pekey et al. 2010; Ergul & Karademir 2020). In addition, Istanbul, a metropolitan city, is a very prominent source of anthropogenic pollution (Altuğ et al. 2009; Mol & Üçok Alakavuk 2011). Another cause of concern in regards to pollution is road and sea traffic. Since the Sea of Marmara is located between the Black Sea and the Aegean Sea, it is a region where maritime traffic is intense (Türk-Çulha et al. 2016). More than 42,553 total ships pass through the Turkish Straits annually (Kutluk 2018). The Pb in the fuel and bilge water that is discharged from ships increases the metal pollution in the Straits (Türk-Çulha et al. 2016). In particular, the heavy metal pollution carried to the Mediterranean by upper currents from the Dardanelles Strait is greater than the pollution carried to the Black Sea by lower currents. It is stated that rising heavy metal pollution in the Dardanelles Strait is caused by wastewater disrupting the stability of the aquatic environment (Süren et al. 2007; Altuğ et al. 2009). The variable water structure in the Sea of Marmara may have contributed to the accumulation of heavy metal pollution in the gulf and coastal areas. In the statistical analysis, significant differences were found in the heavy metal concentration values in all months (
Heavy metal levels in
Site | Cd | Cu | Pb | Ni | Zn | Fe | Reference |
---|---|---|---|---|---|---|---|
Aegean Sea | 0.004 – 0.065 | Nd - 0.249 | 0.010 – 0.191 | 0.021 – 0.339 | 0.26 – 1.66 | 1.85 – 76.0 | Aydın - Önen & Öztürk (2017) |
Mediterranean Sea | 3.9 – 80.0 | 1.6 – 25.0 | 4.9 – 26.1 | 2.0 – 54.2 | 22.7 – 756.8 | 121.3 – 1274 | Duysak & Azdural (2017) |
Black Sea | 0.02 – 0.04 | 0.61 – 0.85 | 0.05 – 0.19 | - - | 12 – 23 | 21 – 38 | Bat et al. (2015) |
Mediterranean Sea | 0.24 – 0.68 | 1.09 – 5.58 | 0.05 – 0.70 | 0.39 – 1.60 | 3.70 – 13.71 | 36.56 – 212.9 | Yüzereroğlu et al. (2010) |
Mediterranean Sea | 0.11 – 2.04 | - - | 0.00 – 3.74 | - - | - - | - - | Ayas et al. (2009) |
Mediterranean Sea | 2.39 – 4.97 | 1.58 – 4.02 | 4.28 – 14.53 | 3.60 - 12.21 | 23.13 – 46.59 | 15.34 – 41.20 | Türkmen et al. (2005) |
Mediterranean Sea | 2.5 – 30.3 | 1.4 – 13.7 | 0.3 – 3.2 | 2.5 – 14.6 | 44.8 – 96 | 891 – 1512 | Ramelov (1985) |
Favignana Island (Italy) | 3.30 – 6.30 | 1.21 – 2.35 | 0.14 – 1.52 | - - | 3.5 – 14.6 | - - | Campanella et al. (2001) |
Saronic Gulf (Greece) | - - | 5.0 – 77.4 | - - | 6.0 – 31.6 | 43 – 367 | 96 – 3045 | Kontopoulos et al. (2003) |
Nord Coasts of Tunisia | 0.43 – 1.50 | 5.59 – 9.29 | 2.73 – 3.61 | 3 – 4.14 | - - | 1.86 – 2.59 | Belkhodja et al. (2010) |
Tunisian Coastal | 0.78 – 1.63 | 5.59 – 9.29 | 3.51 – 3.61 | 3 – 3.43 | - - | 1.86 – 2.59 | Belkhodja & Romdhane (2013) |
Larymna Bay (Greece) | 7.2 – 95.8 | - - | - - | 38.1 – 126 | 843 – 1623 | Bordbar et al. (2015) | |
Favignana Island (Italy) | 1.7 – 11.8 | 0.47 – 3.79 | 0.06 – 2.18 | - - | 2.2 – 19.1 | - - | Cubbada et al. (2001) |
Tyrrhenian Sea (Italy) | 2.89 – 4.06 | 10.2 – 19.2 | 0.51 – 1.50 | - - | 87.4 – 117.1 | - - | Conti and Cecchetti (2003) |
Red Sea | 0.63 – 2.13 | 1.61 – 12.17 | 6.23 – 70.91 | 3.06 – 9.88 | 56.47 – 191.42 | 1.24 – 2.94 | Hamed & Emara (2006) |
North East Greece | - - | 6 – 28 | 8 – 96 | 9 | 196 – 948 | - - | Kelepertsiz (2013) |
The heavy metal concentrations in the
Many bioindicators used to determine the degree of pollution in the environment can have economic characteristics and can make a great contribution to the country's economy through export, though some limitations should be considered in the context of quality control of exported products and safe food consumption. Limiting values may vary depending on the country. Accordingly, the maximum allowable limits for mollusks were compared with those specified by the FDA (2001), the EU (2008), and the TFC (2008). For Cd, the FDA level is 0.2 mg kg−1 (2001), the EU limit is 0.05–1 mg/kg−1 (2008), and the TFC level is 1 mg kg−1 (2008). The Cd values obtained for this study in all months were higher than those limits. The value for Pb is 1.5 mg kg−1 according to all three regulatory bodies. The legal consumable limits specified by the FDA (2001) for Zn and Cu are 150 and 100 mg kg−1, respectively. The measured concentrations of Zn and Cu in all months were lower than these values. Since no limit was specified for Ni and Fe, a comparison could not be made.
The seafood consumption value for an adult was used to calculate the EDI and EWI values for
ADI, PTWI, EDI, EWI, THQ, THQ, and CR estimates for individual heavy metals caused by the consumption of
Heavy Metals | Max. (mg kg−1) | ADI (mg kg−1) | PTWI (mg kg−1) | EDI (mg kg−1) | EWI (mg kg−1) | THQ | TTHQ | CR (mg kg−1) |
---|---|---|---|---|---|---|---|---|
5.74 | 0.06 | 0.44 | 0.002 | 0.014 | ||||
12.90 | 35 | 245 | 0.004 | 0.025 | 0.11 | |||
1.95 | 0.25 | 1.75 | 0.001 | 0.007 | 0.16 | 5.4 10−6 | ||
154.67 | 0.35 | 2.45 | 0.050 | 0.350 | ||||
109.57 | 70 | 490 | 0.036 | 0.252 | 0.12 | |||
3086 | 56 | 392 | 1.005 | 7.035 |
THQ is used to express the risk of non-carcinogenic effects of metals and is a useful parameter for assessing the health risks associated with foods contaminated by heavy metals (Jezierska & Witeska 2006; Abdallah 2013). For this study, RfDs were also used to calculate the THQ values for local residents living in coastal areas, taking into account the maximum heavy metal concentrations in
Another parameter is CR, which is used to calculate the cancer risk in people exposed to heavy metal pollution through consumption. CR values less than 10−6 indicate a negligible carcinogenic risk, while those above 10−4 are unacceptable, according to the USEPA (2010), and those between 10−6 and 10−4 are generally considered acceptable (Fryer et al. 2006). The CR values calculated in the study are given in Table 4. The CPSo values given by the USEPA (2020) for Cd, Pb, and Ni are 6.30, 0.0085, and 1.7, respectively. The CR value for Pb is lower than the limit specified as carcinogenic. Nonetheless, the CR values for Cd and Ni were above the acceptable limits, indicating a potential health hazard for humans consuming
This is the first study on