Abstract
Although fish is widely consumed by humans for its nutritional properties, accumulation of heavy metals can pose serious health hazards. Widespread common carp Cyprinus carpio is cultured worldwide and represents an economically important species for fisheries in several countries. These include Turkey, where C. carpio often makes for a large part of the sales of the locally marketed fish and also for a traditional dish. This study provides a review of bioaccumulation of metals in tissues of C. carpio from water bodies of Anatolia and also includes reference to worldwide studies. From 42 water bodies across the region, 27 metals in total were studied, of which Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn were the most widely analysed, mainly in the muscle, liver and gill tissues. Amongst the potentially toxic metals, Cd, Cr and Pb occurred in several water bodies at concentrations not only above maximum allowed limits but also higher relative to other water bodies worldwide, even though As, Hg and Ni were also sometimes present at potentially hazardous concentrations. The essential metals Cu, Fe, Mn, Se and Zn were detected at various concentrations, with the latter two occasionally above limit. All water bodies flagged as having especially critical (i.e. above limit) concentrations of toxic metals supported C. carpio fisheries from highly populated regions, raising concern about food safety and calling for preventative measures. Given the significantly lower bioaccumulation levels in the muscle relative to the liver and gill tissues, it is suggested that consumption of C. carpio as fillets may be safer than after processing into e.g. meat balls and sausages. The limits of 1.0 μg/g for Cr and 1.15 μg/g for Se, currently lacking from the Turkish food safety legislation, are proposed, and it is suggested that a similar meta-analytical approach as adopted in this study may benefit other countries where C. carpio represents an important fisheries resource.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
Fish is widely consumed by humans for its high content in protein and omega-3 polyunsaturated fatty acids, which help abate cholesterol levels and consequently the risk of certain types of cancer and cardiovascular diseases (Storelli 2008). However, teleost fishes are known to accumulate heavy metals (hereafter, ‘metals’ including metalloids: Duffus 2002) in their body by direct uptake from water (via gills) and through diet. Although there can be considerable variability in bioaccumulation amongst fish species depending on life history (Short et al. 2008), the levels of certain metals in fish tissues generally reflect those found in their biotic and abiotic environments (Birge et al. 2000; Wang and Rainbow 2008). Not surprisingly, a high content of heavy metals (mainly, potentially toxic ones such as As, Cd, Cr, Hg, Ni, Pb, but also essential ones such as Cu, Fe, Mn, Se, Zn, if present at elevated concentrations) may lead to severe threat to fish. This, in turn, can represent a serious health hazard for human consumption (Sorensen 1991; Tüzen 2003; Blanco-Penedo et al. 2006).
The common carp Cyprinus carpio is the most widely distributed freshwater fish worldwide (Vilizzi 2012). It represents a major resource for aquaculture production in several countries (http://www.fao.org/fishery/culturedspecies/Cyprinus_carpio/en), makes for valuable and productive fisheries (e.g. Shumka et al. 2008; Harlioğlu 2011) and is sometimes appreciated as a traditional ethnic dish (Balon 1974). In Turkey, C. carpio is native to the ecoregions (sensu Abell et al. 2008) of Thrace, northern Anatolia, western Transcaucasia and upper Tigris and Euphrates (Memiş and Kohlmann 2006; Vilizzi 2012). However, following translocations since the 1960s (Innal and Erk’akan 2006; Çetinkaya 2010; Tarkan et al. 2015), C. carpio is now widespread throughout the rest of the region, where it represents the most important species for inland fisheries (Turkish Statistical Institute 2014). Indeed, stocking of C. carpio by local government agencies especially into newly established (artificial) reservoirs (e.g. Özuluğ et al. 2005; Balık and Ustaoğlu 2006; Önsoy et al. 2011) is common practice, and also provides for an alternative source of revenue for local communities to compensate for the economic losses resulting from private land encroachment following reservoir construction (Gaygusuz et al. 2015; Tarkan et al. 2015).
Traditionally, in Turkey C. carpio has represented a favourite dish especially in the regions of central and eastern Anatolia, where it makes for a large part of the sales of the locally marketed fish (e.g. Orsay and Duman 2008a). To improve the quality of the product for human consumption, studies have therefore investigated the physicochemical and microbiological characteristics of smoked (mirror) C. carpio fillets (Patir and Duman 2006; Duman and Dartay 2007; Duman and Patir 2007; Can et al. 2011), as well as the processing of its flesh into meat balls and sausages (Yanar and Fenercioğlu 1999; Arslan et al. 2001; Can and Coban 2012).
Clearly, given the importance of C. carpio as a food resource in Turkey, it is imperative that a deeper understanding should be gained on the safety of this fish as a consumer’s product, including knowledge of those water bodies sustaining profitable fisheries but more prone to pollution-induced hazards. The objective of the present study was to provide a synthesis on bioaccumulation of metals in C. carpio from water bodies of the region. Based on an extensive review of the literature: (i) a quantitative evaluation was made of the concentration of various metals in body tissues of C. carpio and relative, whenever possible, to established maximum allowed limits for human consumption; (ii) water bodies of the region with above-limit concentration of metals in C. carpio tissues were identified and flagged according to their level of contamination; and (iii) a comparison was made with bioaccumulation of metals in C. carpio tissues from water bodies worldwide with the aim to cast the outcomes of the present study within a global perspective. It is recommended that measures be implemented for enhancing the safety of C. carpio fisheries of the region for human food consumption.
Material and methods
Data collation
Bioaccumulation data for C. carpio in Anatolia were obtained from peer-reviewed papers, thesis dissertations and, occasionally, conference proceedings. A necessary criterion for inclusion of a study into the review was that it should deal with C. carpio sampled under natural conditions. For this reason, laboratory-based (bioassay) studies carried out in situ (Kargın and Erdem 1991; Canlı and Kargın 1995; Barlas 1999b; Cicik 2003; Karaytug et al. 2007; Çoban et al. 2013; Cogun and Kargın 2013; Yeşilbudak and Erdem 2013, 2014) or on fish sampled from one or more water bodies under monitoring (Ozkurt 2000; Sahan et al. 2010; Uysal et al. 2010; Güngördü et al. 2012) were not included. Notably, the dataset provided by Küçükbay and Örün (2003) for Karakaya Reservoir was excluded because of the unrealistic concentration values provided; whereas the study by Çiçek and Koparal (2001) did not present data in a format suitable for analysis and that by Yaman et al. (2013), albeit reporting average concentration values for some metals, relied on samples of C. carpio pooled across several water bodies.
The same criterion used for selection of the Turkish-based studies was applied to bioaccumulation data for C. carpio worldwide. In this case, the studies by Yousafzai et al. (2012) for Kabul River, Pakistan, and by Gummadavelli et al. (2013) for Edulabad Reservoir, India, were excluded from analysis due to unrealistically high values reported. Similarly, the study by Zubcov et al. (2012) from Dubasari Reservoir in Moldova was excluded because of metal concentration values provided only for gonads (i.e. not muscle, liver and/or gill).
Data preparation
For each study from Anatolia, information was retrieved about the water body under investigation, which was classified into artificial reservoir, natural lake or water course. For both the Anatolian and worldwide studies, the concentration of metals analysed for bioaccumulation and the type of tissue examined were then recorded, even though metals present at levels below detection (with limits determined depending on the individual study) were excluded from the dataset. This was because the aim of the present study was to provide a ‘quantitative’ rather than a ‘methodological’ review, but also for reasons of parsimony in the presentation of results (e.g. Patiño et al. 2013) and considering that ‘blank’ values would have not affected the outcomes of the meta-analysis. Overall, this ensured equality control and quality assurance of the methods utilised in the reviewed studies. Further, despite early attempts, no grouping of metals into ‘classes’ was made because of inconsistencies in their classification (see Nieboer and Richardson 1980; Duffus 2002; Mahboob 2013). In case of studies with replicated spatial (i.e. site level) and/or temporal (i.e. seasonal, monthly) sampling or dealing with C. carpio scale variants (i.e. scale, mirror) or different sexes, the mean concentration value of a metal was taken for the comparative analyses. The same criterion was applied to studies carried out in the same water body by different authors.
Owing to concentration measurements being reported in different forms (i.e. mg/g, mg/kg, μg/g, μg/kg, ppm) and to μg/g being taken as the reference measure in the present study due to its wider employment throughout the reviewed literature, the following relationship was used for conversion:
Similarly, being wet weight most commonly reported across studies than dry weight, the following relationship was used (after Sorensen 1991):
Finally, whenever possible, the maximum allowed limit for concentration of a metal was obtained from the Turkish Food Codex (TFC 2002, 2011) and, if not provided therein, from FAO guidelines (Nauen 1983), with values averaged over all countries for which it was reported. Notably, except for As, Cu and Zn, for which the limits provided in the reviewed studies reporting such values were in agreement with those specified in the TFC, those for other metals were defined based on a combination of the latter whereby the selected value was set following a ‘precautionary approach’.
Statistical analysis
Differences in mean concentration amongst waterbody types (i.e. artificial reservoirs, natural lakes and water courses) and the most widely analysed tissues (i.e. muscle, liver and gill) for the eight most studied metals (i.e. Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn) on C. carpio in Anatolia were tested by permutational univariate analysis of variance (PERANOVA). This was based on a three-way (fully-crossed) design, which included the fixed factors waterbody type, tissue and metal. Analysis was carried out in PERMANOVA + v1.0.1 for PRIMER v6.1.11 (Anderson et al. 2008) following normalisation of the data, using a Euclidean distance and 9999 permutations of the raw data (Anderson and Robinson 2001), and with statistical effects (including a posteriori pair-wise comparisons, in case of significance) evaluated at α = 0.05. Briefly, the advantage of PERANOVA compared to traditional parametric analysis of variance is that the stringent assumptions of normality and homoscedasticity, which proved very often unrealistic when dealing with ecological datasets, are ‘relaxed’ considerably.
For the worldwide comparison, the mean values of the eight most studied metals (as above) were assessed against those for C. carpio from water bodies worldwide by means of quartile analysis (computed under Excel® 2013 as: Q0 = minimum; Q1 = lower quartile or 25th percentile; Q2 = second quartile or 50th percentile; Q3 = third quartile or 75th percentile; Q4 = maximum). Notably, quartiles were computed based on the mean concentration values of each metal from the water bodies worldwide. The waterbody-specific concentration values for C. carpio in Anatolia were then ranked from 0 to 4 according to the quartile into which they fell.
Results
Based on the 43 studies in total selected for review, bioaccumulation data were retrieved for C. carpio sampled from 42 water bodies across Anatolia (Table 1). In total, 27 metals (Table 1) were analysed for concentration from twelve tissues of carp (Appendix Table A1). Amongst metals, Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn were the most widely analysed; amongst tissues, the muscle, liver and gill were the most commonly used (Appendix Table A2). Maximum allowed limits were provided by the TFC for As, Cd, Cu, Hg, Pb and Zn, and worldwide by FAO for Cr and Se (Appendix Table A2). Of the eight most studied metals, Cd, Cr and Pb occurred in the muscle, liver and gill in concentrations above or well above the maximum allowed limit in several water bodies, and the same was true for Zn except for the muscle tissue (Fig. 1). On the contrary, Cu was always present in concentrations below limit, whereas no limits were available for Fe, Mn and Ni, whose concentrations varied from (comparatively) high to (comparatively) low across the water bodies in which they were studied. Of the lesser-studied metals for which a limit was available, As occurred above threshold in two of the three water bodies where it was investigated, similar to Se, whereas Hg occurred at concentrations above limit in only one waterbody, and its detection was limited to the muscle tissue (Fig. 2).
Across Anatolia, amongst the metals for which maximum allowed limits were available, only Cu and Hg always occurred below threshold at overall mean concentrations (i.e. averaged over muscle, liver and gill tissues). Conversely, concentrations of Cd and Pb were above limit in 18 and 20 water bodies, respectively (out of the 42 in total investigated), that of Cr and Zn in six and ten water bodies, respectively, and that of As and Se in one water body (namely, Bafra Balık Lakes) in each case (Fig. 3). Overall, in 27 of the water bodies examined (equal to 67.5 % of the total) C. carpio was found to have one or more metals in overall mean concentrations above limit. Specifically, Bafra Balɪk Lakes and Işıklı Reservoir were the water bodies with the largest number (n = 4) of such metals at critical concentrations, namely As, Cd, Se and Zn for the former and Cd, Cr, Pb and Zn and for the latter. Of the other water bodies, six (22 % of total) had three metals, ten (37 %) two metals and the other nine (33 %) one metal above limit (Fig. 4).
For the eight most investigated metals, there were no significant differences in their mean concentration amongst waterbody types, but there were differences amongst tissues depending on the metal (Table 2). Specifically, the mean concentrations of Cu, Fe, Pb and Zn (with the latter two metals above limit) were always significantly higher in the liver relative to muscle tissue and, except for Cu, the same was true for the gill relative to muscle tissue (Fig. 5). Conversely, there were no significant differences in the concentration amongst tissues for Cd, Cr, Mn and Ni.
Worldwide, based on 56 studies in total (Table 3), bioaccumulation data for C. carpio were retrieved for 102 water bodies across 23 countries. Upon comparison with the worldwide dataset (Table 3): for Cd, eight out of 18 Anatolian water bodies had concentration values (muscle, liver and/or gill tissues combined) above Q2, of which three within Q3 and the other five within Q4; for Cr, five out of six Anatolian waterbodies had concentration values above Q2, of which one within Q3 and the other four within Q4; for Pb, nine out of 20 Anatolian water bodies had concentration values above Q2, of which four within Q3 and the other five within Q4; for Se, only one water body (namely, Bafra Balɪk Lakes) had a critical value within Q0; and for Zn, four out of ten Anatolian water bodies had concentration values above Q2, of which three within Q3 and the other one within Q4 (Fig. 6).
In total, in 16 out of the 42 water bodies examined (equal to 38 %) C. carpio was found to have one or more metals in a concentration (muscle, liver and/or gill tissues combined) within or above Q3 (Fig. 7). Specifically, Beyşehir Lake together with Demirköprü and Işıklı reservoirs were the water bodies with the largest number (n = 3) of metals at critical concentrations, and specifically Cd, Cr and Pb. Of the other water bodies, six (31 % of total) had two metals and the remaining eight (50 %) one metal within or above Q3.
Discussion
Similar to other biological aspects of C. carpio investigated for Turkey (Vilizzi et al. 2013, 2014a, b, 2015a, b), the dense matrix of studies available at the country level has provided an extensive dataset from which to draw general conclusions about the extent of bioaccumulation of metals in C. carpio tissues. Cd, Cr and Pb were the toxic metals that occurred in several cases at concentrations not only above maximum allowed limits but also comparatively higher relative to other water bodies worldwide. Other toxic metals such as As, Hg and, possibly, Ni also were present in some cases at potentially hazardous concentrations. Whereas, the essential metals Cu, Fe, Mn, Se and Zn were detected at various concentrations, with the latter two in some cases above limit. Overall, the present findings warrant careful evaluation given that C. carpio is caught throughout the country (Harlioğlu 2011) and represents in most areas an important food resource (Turkish Statistical Institute 2014).
Amongst the metals regarded as toxic (and studied more extensively in Turkey): cadmium (Cd) injures the kidney and causes symptoms of chronic toxicity, including impaired kidney function, poor reproductive capacity, hypertension, tumours and hepatic dysfunction (Waalkes 2000); chromium (Cr + 6), despite being in some cases a nutrient essential to glucose metabolism, at higher doses may cause severe environmental and public health problems and is considered a carcinogenic and mutagenic substance for humans (Rowbotham et al. 2000); lead (Pb) is known to be toxic for the brain, kidney and reproductive system and can also cause impairment in intellectual functioning, fertility, miscarriage and hypertension (Flora 2002; Yaman 2006); arsenic (As) can cause acute and chronic toxicity and turn minor disorders into cancer and even death (Bhattacharya et al. 2007); mercury (Hg) is highly toxic in metabolically active tissues causing high ecotoxicological risks (Pelletier 1995); finally, nickel (Ni), despite its being a moderately toxic element, when present in high concentrations in food may be responsible for a number of diseases (Schiavino et al. 2006).
Amongst the metals regarded as essential (and studied more extensively in Turkey): copper (Cu) is known to play a role in the activation of some important enzymes, so that changes in concentration may cause various metabolic alterations (Ozen et al. 2002); iron (Fe) plays an important role in fighting anaemia, which is not uncommon in children and women across Turkey (Walter et al. 1998); manganese (Mn) is a vital trace metal for the functioning of many organic systems where it plays a major role in the regulation of blood sugar and reproduction, digestion, and bone growth and also acts as a cellular antioxidant (Aschner and Aschner 2005); selenium (Se) has attracted attention because of its antioxidant properties, thereby protecting cells from damage (Sorensen 1991); finally, zinc (Zn) is an important trace element in human metabolism and nutrition and plays a major role in the functioning of many biochemical processes (Scherz and Kirchhoff 2006).
Contrary to ponds and water courses, which are generally subjected only to limited angling activities and exploitation mainly related to sport fishing, reservoirs and large natural lakes in Turkey are usually targeted by professional fishing cooperatives (but also amateur fishermen), with the rate of exploitation becoming more intense in the vicinity of highly populated areas. This is the case of e.g. Almus Reservoir (Zengin and Buhan 2007), Keban Reservoir (Celayir et al. 2006; Orsay and Duman 2005, 2008b; Yüngül et al. 2012), Menzelet Reservoir (Alp et al. 2003), Seyhan Reservoir (Ozyurt et al. 2004; Çiçek et al. 2006; Mete and Yüksel 2014) and Lake Eğirdir (Balık et al. 2007). All these water bodies support productive C. carpio fisheries and were flagged in the present study as having critical levels of certain toxic metals in C. carpio tissues.
Based on the current review, an even more critical situation was identified for Bafra Balɪk Lakes and Işıklı Reservoir (relative to Turkish water bodies) and for Beyşehir Lake (relative to water bodies worldwide), and this was due to elevated concentrations of both toxic and essential metals. Notably, Işıklı Reservoir is located in populated Denizli Province and supports cooperative-based fishing exploitation of C. carpio (Eren and Tenekecioğlu 2006), whereas Beyşehir lake (which is located in the city of Konya) is known to support very large catches of C. carpio (Balık and Çubuk 2004).
Bafra Balık Lakes also were flagged in the present study as yielding high concentrations of toxic As (but also essential Se and Zn) in C. carpio tissues. This lake system consists of 33 small water bodies located in Samsun Province, where C. carpio also represents a favourite local dish. Contrary to artificial reservoirs, with their typical V-shaped profile and high depth resulting in a restricted littoral zone area, this type of water bodies provides for extensive shallow and vegetated areas ideal for successful spawning of C. carpio (Balon 1995). In this respect, it has been argued that, if successful stocking of C. carpio and related productive fisheries are to be achieved, shallow (natural) lakes in general should be targeted as potential alternative waterbodies to reservoirs (Gaygusuz et al. 2015). As Bafra Balık Lakes does represent one such potential area in a country with overall limited availability of shallow water bodies, the finding of elevated metal concentrations in the feral population of C. carpio in these lakes raises concerns not only about the feasibility of suggested potential stocking alternatives but also about the safety of C. carpio consumed locally as food.
The significantly higher concentrations of some metals (namely, Cu, Fe, Pb and Zn) in the liver (but also gill) relative to the muscle tissue are in line with findings from other studies, which indicate that the liver and gill are metabolically active and accumulate metals in higher levels relative to the muscle, not only in C. carpio (e.g. Velcheva 2006; Alhashemi et al. 2012; Ardakani and Jafari 2014) but more generally in fish (Allen 1994, 1995; Spehar et al. 1998). This is because, unlike other tissues, the muscle does not come into direct contact with metals as it is covered externally by the skin and also does not function as an active site for detoxification (hence transport of trace metals to other tissues). Further, as regards food processing, this finding is noteworthy as it may have important implications for health and food safety should the preparation of meat balls and sausages from C. carpio involve the utilisation of body parts other than the muscle (fillet).
Unlike the many studies (both Turkey-based and worldwide, and reviewed herein) on C. carpio bioaccumulation that have focused on individual water bodies, to the author’s knowledge, the present review has been the first one to provide a country-level synthesis and evaluation of the topic. This is important if guidelines are to be provided for the management of sustainable and healthy fisheries and related legislation is to be amended/implemented. To this end, a similar meta-analytical approach as the one used in the current study is suggested for other countries where C. carpio represents an important resource for fisheries. This could be the case for e.g. Iran, where in the last two decades the per capita consumption of fish (including C. carpio) has increased sharply (Ebrahimi and Taherianfard 2011), and for which the second largest number of bioaccumulation studies (after Turkey) was retrieved in this review (Table 3).
At the country level, the present findings indicate that there is a pressing need to re-evaluate the status of C. carpio fisheries in most water bodies, and especially those located in the proximity of highly populated areas due to potentially excessive levels of bioaccumulated metals that may ultimately pose a risk to human health. As the current TFC does not include limits for toxic Cr, the value of 1.0 μg/g suggested in the present study may be included in future legislation and the same could apply to the value of 1.15 μg/g for (essential) Se. Finally, within a broader international context, the current synthesis and evaluation study on bioaccumulation of metals in (edible) C. carpio in Turkey will help contribute to the improvement of the country’s food safety policy, so as to align with e.g. expected European Commission standards (European Commission 2013).
References
Abell, R., Thieme, M. L., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Contreras Balderas, S., Bussing, W., Stiassny, M. L. L., Skelton, P., Allen, G. R., Unmack, P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., Higgins, J. V., Heibel, T. J., Wikramanayake, E., Olson, D., López, H. L., Reis, R. E., Lundberg, J. V., Sabaj-Pérez, M. H., & Petry, P. (2008). Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. BioScience, 58(5), 403–414.
Alam, M. G. M., Tanaka, A., Allinson, G., Laurenson, L. J. B., Stagnitti, F., & Snow, E. T. (2002). A comparison of trace element concentrations in cultured and wild carp (Cyprinus carpio) of Lake Kasumigaura, Japan. Ecotoxicology and Environmental Safety, 53(3), 348–354.
Alhashemi, A. H., Sekhavatjou, M. S., Kiabi, B. H., & Karbassi, A. R. (2012). Bioaccumulation of trace elements in water, sediment, and six fish species from a freshwater wetland, Iran. Microchemical Journal, 104, 1–6.
Allen, P. (1994). Accumulation profiles of lead and the influence of cadmium and mercury in Oreochromis aureus (Steindacher) during chronic exposure. Toxicological & Environmental Chemistry, 44(1–2), 101–112.
Allen, P. (1995). Chronic accumulation of cadmium in the edible tissues of Oreochromis aureus (Steindacher): modification by mercury and lead. Archives of Environmental Contamination and Toxicology, 14(1), 193–196.
Alp, A., Büyükçapar, H. M., & Eren, A. (2003). Commercially fish species and their fisheries in Menzelet Dam Lake (Kahramanmaraş). KSU Journal of Science and Engineering, 6(2), 142–153. In Turkish with an English abstract.
Altındağ, A., & Yiğit, S. (2005). Assessment of heavy metal concentrations in the food web of lake Beyşehir, Turkey. Chemosphere, 60(4), 552–556.
Al-Weher, S. M. (2008). Levels of heavy metal Cd, Cu and Zn in three fish species collected from the northern Jordan valley, Jordan. Jordan Journal of Biological Sciences, 1(1), 41–46.
Anderson, M. J., & Robinson, J. (2001). Permutation tests for linear models. Australian & New Zealand Journal of Statistics, 43(1), 75–88.
Anderson, M. J., Gorley, R. N., & Clarke, K. R. (2008). PERMANOVA+ for PRIMER: Guide to software and statistical methods (p. 214). Plymouth, UK: PRIMER-E Ltd.
Ardakani, S. S., & Jafari, S. M. (2014). Assessment of heavy metals (Cu, Pb and Zn) in different tissues of common carp (Cyprinus carpio) caught from Shirinsu Wetland, Western Iran. Journal of Chemical Health Risks, 4(2), 47–54.
Ardakani, S. S., & Jafari, S. M. (2015). Metals analysis in common carp (Cyprinus carpio) from Shirinsu Wetland, Hamedan province, Iran. Archives of Hygiene Sciences, 4(4), 172–178.
Ariyaee, M., Azadi, N. A., Majnoni, F., & Mansouri, B. (2015). Comparison of metal concentrations in the organs of two fish species from the Zabol Chahnimeh Reservoirs, Iran. Bulletin of Environmental Contamination and Toxicology, 94(6), 715–721.
Arslan, A., Dinçoğlu, A. H., & Gönülalan, Z. (2001). Fermented Cyprinus carpio L. sausage. Turkish Journal of Veterinaty and Animal Science, 25(5), 667–673.
Aschner, J. L., & Aschner, M. (2005). Nutritional aspects of manganese homeostasis. Molecular Aspects of Medicine, 26(4–5), 353–362.
Asgedom, A. G., Desta, M. B., & Gebremedh, Y. W. (2012). Bioaccumulation of heavy metals in fishes of Hashenge Lake, Tigray, Northern Highlands of Ethiopia. American Journal of Chemistry, 2(6), 326–334.
Ayaş, Z., & Kolankaya, D. (1996). Accumulation of some heavy metals in various environments and organisms at Göksu Delta, Türkiye, 1991–1993. Bulletin of Environmental Contamination and Toxicology, 56(1), 65–72.
Ayas, Z., Ekmekci, G., Yerli, S. V., & Ozmen, M. (2007). Heavy metal accumulation in water, sediments and fishes of Nallihan Bird Paradise, Turkey. Journal of Environmental Biology, 28(3), 545–549.
Aydın, D., & Coskun, O. F. (2013). Concentrations of some heavy metals in water, sediment and some living organisms from the Zamanti River in Turkey. Internatıonal Journal of Natural and Engineering Sciences, 7(3), 56–62.
Babaei, H., & Khodaprast, S. H. (2013). Evaluating the contamination of heavy metals in sediment of fish (Cyprinus carpio) from Anzali international wetland, Giulan. KAUMS Journal (FEYZ), 16(7), 667–668. In Persian with an English abstract.
Balık, S., & Çubuk, H. (2004). Effect of net twine on efficiency of trammel nets for catching carp (Cyprinus carpio Linnaeus, 1758) in Lake Beyşehir and silver crucian carp (Carassius gibelio Bloch, 1782) in Lake Eğirdir. Turkish Journal of Fisheries and Aquatic Sciences, 4, 39–44.
Balık, S., & Ustaoğlu, M. R. (2006). Results of fish introduction studies in lakes, ponds and reservoirs of Turkey. 1. Fish Stocking and Reservoir Management Symposium, 07–09 February 2006, Antalya, Turkey.
Balık, I., Cubuk, H., & Ozkök, R. (2007). Spatial distributions of economic fish populations in Lake Eğirdir. Journal of Fisheries Sciences, 1(2), 88–96. In Turkish with an English abstract.
Balon, E. K. (1974). Domestication of the carp Cyprinus carpio L (p. 37). Toronto: Royal Ontario Museum Life Sciences Miscellanous Publication.
Balon, E. K. (1995). The common carp, Cyprinus carpio: its wild origin, domestication in aquaculture, and selection as colour nishikigoi. Guelph Ichthyology Reviews, 3, 1–55.
Barlas, N. (1999a). A pilot study of heavy metal concentration in various environments and fishes in the upper Sakarya River Basin, Turkey. Environmental Toxicology, 14(3), 367–373.
Barlas, N. (1999b). Histopathological examination of gill, liver and kidney tissues of carp (Cyprinus carpio L., 1758) fish in the Upper Sakarya River Basin. Turkish Journal of Veterinary and Animal Sciences, 23(2), 277–284. In Turkish with an English abstract.
Benzer, S., Arslan, H., Uzel, N., Gül, A., & Yılmaz, M. (2013). Concentrations of metals in water, sediment and tissues of Cyprinus carpio L., 1758 from Mogan Lake (Turkey). Iranian Journal of Fisheries Sciences, 12(1), 45–55.
Bhattacharya, P., Welch, A. H., Stollenwerk, K. G., McLaughlin, M. J., Bundschuh, J., & Panaullah, G. (2007). Arsenic in the environment: biology and chemistry. Science of the Total Environment, 379(2–3), 109–120.
Birge, W. J., Price, D. J., Shaw, J. R., Spromberg, J. A., Wigginton, A. J., & Hogstrand, C. (2000). Environmental Toxicology and Chemistry, 19(4), 1199–1212.
Blanco-Penedo, I., Cruz, J. M., López-Alonso, M., Miranda, M., Castillo, C., Hernández, J., & Benedito, J. L. (2006). Influence of copper status on the accumulation of toxic and essential metals in cattle. Environment International, 32(7), 901–906.
Çağlar, C. (2010). Determination of heavy metals in liver, gill and muscle tissues of Phoxinellus anatolicus Hanko, 1924 and Cyprinus carpio Linneaus, 1758 living in Suğla Lake. MSc Thesis, Selçuk University, Konya, Turkey, 79 pp. [In Turkish with an English abstract]
Can, O. P., & Coban, O. E. (2012). The effect of thyme on the storage time of fish balls prepared from mirror carp (Cyprinus carpio carpio L.,1758). Journal of Etlik Veterinary Microbiology, 23(1), 9–14. In Turkish with an English abstract.
Can, P. Ö., Yalçin, H., & Arslan, A. (2011). Assesment of quality criteria of Cyprinus carpio fillets marinated with eugenole solution for different time. The Black Sea Journal of Sciences, 2(5), 17–27. In Turkish with an English abstract.
Canlı, M., & Kargın, F. (1995). A comparative study on heavy metal (Cd, Cr, Pb and Ni) accumulation in the tissue of the carp Cyprinus carpio and the Nile fish Tilapia nilotica. Turkish Journal of Zoology, 19(2), 165–171.
Canlı, M., Ay, O., & Kalay, M. (1998). Levels of heavy metals (Cd, Pb, Cu, Cr and Ni) in tissue of Cyprinus carpio, Barbus capito and Chondrostoma regium from the Seyhan River, Turkey. Turkish Journal of Zoology, 22(2), 149–158.
Celayir, Y., Pala, M., & Yüksel, F. (2006). Fisheries in Keban Dam Lake. I Balıklandırma ve Rezervuar Yönetimi Sempozyumu, 07–09 February 2006, Antalya, pp. 259–267. [In Turkish with an English abstract.]
Cerveny, D., Zlabek, V., Velisek, J., Turek, J., Grabic, R., Grabicova, K., Fedorova, G., Rosmus, J., Lepic, P., & Randak, T. (2014). Contamination of fish in important fishing grounds of the Czech Republic. Ecotoxicology and Environmental Safety, 109, 101–109.
Çetinkaya, O. (2010). Distribution, ecology and use of common carp (Cyprinus carpio) in Turkey. 1st International Symposium of Fisheries and Fishing Tourism, Zbornik Radova Proceedings, 23–24 June 2010, pp. 173–188.
Chalmers, A. T., Argue, D. M., Gay, D. A., Brigham, M. E., Schmitt, C. J., & Lorenz, D. L. (2011). Mercury trends in fish from rivers and lakes in the United States, 1969–2005. Environmental Monitoring and Assessment, 175(1–4), 175–191.
Chi, Q. Q., Zhu, G. W., & Langdon, A. (2007). Bioaccumulation of heavy metals in fishes from Taihu Lake, China. Journal of Environmental Sciences, 19(12), 1500–1504.
Çiçek, A., Emiroğlu, Ö., & Arslan, N. (2009). Heavy metal concentration in fish of Lake Manyas. In World Lake Conference, Wuhan, China, 1–5 November 2009, 5 pp.
Çiçek, E., Avşar, D., & Özyurt, C. E. (2006). Estimation of the biomass and expoitation rate on the carp (Cyprinus carpio Linnaeus, 1758) and pike-perch (Sander lucioperca Bogustkaya & Naseka, 1996) inhabiting in Seyhan Dam Lake. I Balıklandırma ve Rezervuar Yönetimi Sempozyumu, 07–09 February 2006, Antalya, pp. 179–194. [In Turkish with an English abstract.]
Çiçek, A., & Koparal, A. S. (2001). The levels of lead, chromium and cadmium in the Cyprinus carpio and Barbus plebejus, living in Porsuk Reservoir. Ekoloji Çevre Dergisi, 39(10), 3–6.
Cicik, B. (2003). The effects of copper-zinc interaction on the accumulation of metals in liver, gill and muscle tissues of common carp (Cyprinus carpio L.). Ekoloji, 12(48), 32–36. In Turkish with an English abstract.
Çoban, M. Z., Eroğlu, M., Canpolat, O., Çalta, M., & Şen, D. (2013). Effect of chromium on scale morphology in scaly carp (Cyprinus carpio L.). The Journal of Animal & Plant Sciences, 23(5), 1455–1459.
Cogun, H. Y., & Kargın, F. (2013). The effect of copper and lead on Oreochromis niloticus and Cyprinus carpio in blood ion level. Ekoloji, 87(22), 51–57. In Turkish with an English abstract.
De Regla, E. N., De Leon, M. S., Estrella, E. A., & Duay, B. S. C. (2015). Determination of pH levels and cadmium content of surface, ground water and aquatic life in Bustos, Bulacan, Philippines. International Journal of ChemTech Research, 8(4), 1836–1845.
Derrag, Z., & Youcef, N. D. (2014). Bioaccumulation of heavy metals in the Cyprinus carpio organs of the El Izdihar dam (Algeria). Desalination and Water Treatment, 52(10–12), 2293–2300.
Dirican, S., Yokuş, A., Karaçınar, S., & Durna, S. (2013). Chromium (Cr), nickel (Ni) and zinc (Zn) levels in edible muscle and skin tissues of Cyprinus carpio L. in Çamligöze Dam Lake, Sivas, Turkey. Veterinarija ir Zootechnika, 63(85), 17–22.
Duffus, J. H. (2002). “Heavy metals”: a meaningless term? Pure and Applied Chemistry, 74(5), 793–807.
Duman, M., & Dartay, M. (2007). Changes in meat yield and chemical composition of mirror carp (Cyprinus carpio L., 1758) fillets after hot-smoked. Doğu Anadolu Bölgesi Araştırmaları pp. 186–190. [In Turkish with an English abstract.]
Duman, M., & Patir, B. (2007). The determination of some chemical and sensory characteristics of smoked mirror carp (Cyprinus carpio L.) fillets. Science and Engineering Journal of Fırat University, 19(4), 463–472. In Turkish with an English abstract.
Ebrahimi, M., & Taherianfard, M. (2011). The effects of heavy metals exposure on reproductive systems of cyprinid fish from Kor River. Iranian Journal of Fisheries Sciences, 10(1), 13–26.
Erdoğrul, Ö. (2007). Determination of mercury levels in edible tissues of various fish samples from Sır Dam Lake. Turkish Journal of Biology, 31(4), 197–201.
Erdoğrul, Ö., & Ateş, D. A. (2006). Determination of cadmium and copper in fish samples from Sir and Menzelet Dam Lake Kahramanmaraş, Turkey. Environmental Monitoring and Assessment, 117(1), 281–290.
Erdoğrul, Ö., & Erbilir, F. (2007). Heavy metal and trace elements in various fish samples from Sır Dam Lake, Kahramanmaraş, Turkey. Environmental Monitoring and Assessment, 130(1), 373–379.
Eren, R., & Tenekecioğlu, E. (2006). Studies on limnology, determining of cathable fish stocks and planting with carp fingerlings carried out in Lake Isıklı. I Balıklandırma ve Rezervuar Yönetimi Sempozyumu, 07–09 February 2006, Antalya, pp. 423–429. [In Turkish with an English abstract.]
European Commission (2013). Commission Staff Working Document–Turkey 2013 Progress Report. SWD(2013) 417 final. http://ec.europa.eu/enlargement/pdf/key_documents/2013/package/brochures/turkey_2013.pdf. Accessed 28 December 2015.
Falfushynska, H. I., & Stoliar, O. B. (2009). Function of metallothioneins in carp Cyprinus carpio from two field sites in Western Ukraine. Ecotoxicology and Environmental Safety, 72(5), 1425–1432.
Flora, S. J. S. (2002). Lead exposure: health effects, prevention and treatment. Journal of Environmental Biology, 23(1), 25–41.
Gaygusuz, Ö., Tarkan, A. S., Aydın, H., Dorak, Z., Top, N., Karakuş, U., & Vilizzi, L. (2015). Stocking of common carp (Cyprinus carpio) into newly-established reservoirs may create new introduction pathways for non-native fish. Turkish Journal of Fisheries and Aquatic Sciences, 15(4), 833–840.
Göksu, M. L. Z., Çevik, F., Fındık, Ö., & Sarıhan, E. (2003). Investigation of Fe, Zn and Cd in mirror carp (Cyprinus carpio L., 1758) and pike perch (Stizostedion lucioperca L., 1758) from Seyhan Dam Lake. Ege University Journal of Fisheries and Aquatic Sciences, 20(1–2), 69–74.
Gummadavelli, V., Piska, R. S., Noothi, S., & Manikonda, P. K. (2013). Seasonal bioaccumulation of heavy metals in Cyprinus carpio of Edulabad water reservoir, Andhra Pradesh, India. International Journal of Life Sciences Biotechnology and Pharma Research, 2(3), 127–143.
Güngördü, A., Erkmen, B., & Kolankaya, D. (2012). Evaluation of spatial and temporal changes in biomarker responses in the common carp (Cyprinus carpio L.) for biomonitoring the Meric, Delta, Turkey. Environmental Toxicology and Pharmacology, 33(3), 431–439.
Gurcu, B., Yildiz, S., Koca, Y. B. G., & Koca, S. (2010). Investigation of histopathological and cytogenetic effects of heavy metals pollution on Cyprinus carpio (Linneaus, 1758) in the Gölmarmara Lake, Turkey. Journal of Animal and Veterinary Advances, 9(4), 798–808.
Harlioğlu, A. G. (2011). Present status of fisheries in Turkey. Reviews in Fish Biology and Fisheries, 21(4), 667–680.
Has-Schön, E., Bogut, I., Vuković, R., Galović, D., Bogut, A., & Horvatić, J. (2015). Distribution and age-related bioaccumulation of lead (Pb), mercury (Hg), cadmium (Cd), and arsenic (As) in tissues of common carp (Cyprinus carpio) and European catfish (Sylurus [sic] glanis) from the Buško Blato reservoir (Bosnia and Herzegovina). Chemosphere, 135, 289–296.
Hettige, N. D., Weerasekara, K. A. W. S., Azmy, S. A. M., Wickramarachchi, W. D. N., & Jinadasa, B. K. K. K. (2015). Bioaccumulation of trace metals in Cyprinus carpio (common carp) from Bomuruella Reservoir, Nuwara-Eliya. Journal of Environmental Professionals Sri Lanka, 4(1), 64–71.
Hinck, J. E., Schmitt, C. J., Ellersieck, M. R., & Tillitt, D. E. (2008). Relations between and among contaminant concentrations and biomarkers in black bass (Micropterus spp.) and common carp (Cyprinus carpio) from large US rivers, 1995–2004. Journal of Environmental Monitoring, 10(12), 1499–1518.
İlhak, O. İ., Karatepe, P., & Özçelik, M. (2012). Heavy metal levels in some fish species sold at retail in Elazig. Fırat University Medical Journal of Health Sciences, 26(2), 99–103.
Innal, D., & Erk’akan, F. (2006). Effects of exotic and translocated fish species in the inland waters of Turkey. Reviews in Fish Biology and Fisheries, 16(1), 39–50.
Ioniţă, C., Mititelu, M., & Moroşan, E. (2014). Analysis of heavy metals and organic pollutants from some Danube River fishes. Farmácia, 62(2), 299–305.
Iqbal, J., & Shah, M. H. (2014). Study of seasonal variations and health risk assessment of heavy metals in Cyprinus carpio from Rawal Lake, Pakistan. Environmental Monitoring and Assessesment, 186(4), 2025–2037.
Jabeen, F., & Chaudhry, A. S. (2010). Monitoring trace metals in different tissues of Cyprinus carpio from the Indus River in Pakistan. Environmental Monitoring and Assessment, 170(1–4), 645–656.
Jafari, S. M., & Sobhanardakani, S. (2014). Determination of heavy metal (Cu, Pb and Zn) concentrations in muscle tissue of Hypophthalmichthys molitrix, Cyprinus carpio and Ctenopharyngodon idella caught from Zarivar Wetland, Western Iran. Current World Environment, 9(3), 923–931.
Jarquín-Raymundo, E., Lango-Reynoso, F., Castañeda-Chávez, M. del R., Wakida-Kusunoki, A. T., & Landeros Sánchez, C. (2014). Metales pesados en especies invasoras del sistema fluvio-lagunar-deltaico del río Palizada. Academia Veracruzana de Ciencias Agrícolas, Pecuarias, Forestales Acuícolas y Pesqueras A.C., 20 pp.
Kalyoncu, L., Kalyoncu, H., & Arslan, G. (2012). Determination of heavy metals and metals levels in five fish species from Işıklı Dam Lake and Karacaören Dam Lake (Turkey). Environmental Monitoring and Assessment, 184(4), 2231–2235.
Kandemir, S., Dogru, M. I., Örün, I., Dogru, A., Altas, L., Erdogan, K., Örün, G., & Polat, N. (2010). Determination of heavy metal levels, oxidative status, biochemical and hematological parameters in Cyprinus carpio L., 1758 from Bafra (Samsun) fish lakes. Journal of Animal and Veterinary Advances, 9(3), 617–622.
Kaptan, H., & Tekin-Özan, S. (2014). Determination of the heavy metals levels in some tissues and organs of carp (Cyprinus carpio L., 1758) living in water, sediment of Eğirdir Lake. SDU Journal of Science, 9(2), 44–60.
Karadede, H., & Ünlü, E. (2000). Concentrations of some heavy metals in water, sediment and fish species from the Atatürk Dam Lake (Euphrates), Turkey. Chemosphere, 41(9), 1371–1376.
Karatas, M. (2008). Evaluation of heavy metals in fishes (Cyprinus carpio and Barbus plebejus) of Bedirkale Dam Lake, Turkey. Asian Journal of Chemistry, 20(7), 5741–5744.
Karatas, M., & Seker, Y. (2008). Heavy metal levels in tissues of Cyprinus carpio from Kaz Lake in Tokat, Turkey. Asian Journal of Chemistry, 20(4), 3310–3312.
Karatas, M., Seker, Y., & Sezer, M. (2007). Heavy metal levels of two cyprinid species (Cyprinus carpio and Capoeta trutta) populated in Almus Dam Lake, Turkey. Asian Journal of Chemistry, 19(1), 574–578.
Karaytug, S., Erdem, C., & Cicik, B. (2007). Accumulation of cadmium in the gill, liver, kidney, spleen, muscle and brain tissues of Cyprinus carpio. Ekoloji, 63, 16–22.
Kargın, F., & Erdem, C. (1991). Accumulation of copper in liver, spleen, stomach, intestine, gill and muscle of Cyprinus carpio. Turkish Journal of Zoology, 15(3), 306–314. In Turkish with an English abstract.
Khoshnamvand, M., Kaboodvandpour, S., & Ghiasi, F. (2013). A comparative study of accumulated total mercury among white muscle, red muscle and liver tissues of common carp and silver carp from the Sanandaj Gheshlagh Reservoir in Iran. Chemosphere, 90(3), 1236–1241.
Kır, I., & Tumantozlu, H. (2012). Investigation of some heavy metal accumulation in water, sediment and carp (Cyprinus carpio) samples of Karacaoren-II Dam Lake. Ekoloji, 21(82), 65–70.
Köse, E., & Uysal, K. (2008). Comparison of heavy metal accumulation ratios in muscle, skin and gill of non-mature common carp (Cyprinus carpio L., 1758). Dumlupınar Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 17, 19–26.
Köse, E., Uysal, K., Tokatli, C., Çiçek, A., Emiroğlu, Ö., & Arslan, N. (2012). Assessment of boron in water, sediment and fish tissues of Porsuk Stream, Turkey. Pakistan Journal of Zoology, 44(5), 1446–1449.
Küçükbay, F. Z., & Örün, İ. (2003). Copper and zinc accumulation in tissues of the freshwater fish Cyprinus carpio L. 1758 collected from the Karakaya Dam Lake, Malatya (Turkey). Fresenius Environmental Bulletin, 12(1), 62–66.
Küpeli, T., Altundağ, H., & İmamoğlu, M. (2014). Assessment of trace element levels in muscle tissues of fish species collected from a river, stream, lake, and sea in Sakarya, Turkey. The Scientific World Journal, Article ID 496107, 7 pp.
Luna-Porres, M. Y., Rodríguez-Villa, M. A., Herrera-Peraza, E. F., Renteria-Villalobos, M., & Montero-Cabrera, M. E. (2014). Potential human health risk by metal(loid)s, 234,238U and 210Po due to consumption of fish from the “Luis L. Leon” Reservoir (Northern México). International Journal of Environmental Research and Public Health, 11(7), 6612–6638.
Mahboob, S. (2013). Environmental pollution of heavy metals as a cause of oxidative stress in fish: a review. Life Sciences Journal, 10, 336–347.
Majnoni, F., Rezaei, M., Mansouri, B., & Hamidian, A. H. (2013). Metal concentrations in tissues of common carp, Cyprinus carpio, and silver carp, Hypophthalmichthys molitrix from the Zarivar Wetland in Western Iran. Archives of Polish Fisheries, 21(1), 11–18.
Maktabi, P., Javaheri Baboli, M., Jafarnejadi, A. R., & Askary Sary, A. (2015). Mercury concentrations in common carp (Cyprinus carpio) tissues, sediment and water from fish farm along the Karoun River in Iran. Veterinary Research Forum, 6(3), 217–221.
Maleki, A., Azadi, N. A., Mansouri, B., Majnoni, F., Rezaei, Z., & Gharibi, F. (2015). Health risk assessment of trace elements in two fish species of Sanandaj Gheshlagh Reservoir, Iran. Toxicology and Environmental Health Sciences, 7(1), 43–49.
Mansouri, B., Majnoni, F., Rezaei, Z., & Gharibi, F. (2014). Bioaccumulation of mercury in some organs of two fish species from the Sanandaj Gheshlagh Reservoir, Iran. Journal of Advances in Environmental Health Research, 2(3), 151–156.
Memiş, D., & Kohlmann, K. (2006). Genetic characterization of wild common carp (Cyprinus carpio L.) from Turkey. Aquaculture, 258(1–4), 257–262.
Mendil, D., & Uluözlü, Ö. D. (2007). Determination of trace metal levels in sediment and five fish species from lakes in Tokat, Turkey. Food Chemistry, 101(2), 739–745.
Mendil, D., Uluözlü, Ö. D., Hasdemir, E., Tüzen, M., Sari, H., & Suicmez, M. (2005). Determination of trace metal levels in seven fish species in lakes in Tokat, Turkey. Food Chemistry, 90(1–2), 175–179.
Mendil, D., Ünal, Ö. F., Tüze, M., & Soylak, M. (2010). Determination of trace metals in different fish species and sediments from the River Yeşilırmak in Tokat, Turkey. Food and Chemical Toxicology, 48(5), 1383–1392.
Mert, R., Alaş, A., Bulut, S., & Özcan, M. M. (2014). Determination of heavy metal contents in some freshwater fishes. Environmental Monitoring and Assessement, 186(11), 8017–8022.
Mete, O. S., & Yüksel, F. (2014). The investigation of socio-economic characteristics of commercial and amateur fishery in Seyhan Dam Lake. Bilim ve Gençlik Dergisi, 2(1), 27–42. In Turkish with an English abstract.
Mol, S., Özden, Ö., & Oymak, S. A. (2010). Trace metal contents in fish species from Ataturk Dam Lake (Euphrates, Turkey). Turkish Journal of Fisheries and Aquatic Sciences, 10(2), 209–213.
Nauen, C. E. (1983). Compilation of legal limits for hazardous substances in fish and fishery products (p. 102). Rome: FAO Fisheries Circular - C764.
Nieboer, E., & Richardson, D. H. S. (1980). The replacement of the nondescript term ‘heavy metals’ by a biologically and chemically significant classification of metal ions. Environmental Pollution Series B, Chemical and Physical, 1(1), 3–26.
Nzeve, J. K. (2015). Assessment of Heavy metal contamination in Masinga Reservoir, Kenya. PhD Thesis, Kenyatta University, Kenya, 157 pp.
Ogendi, G. M., Maina, G. M., Mbuthia, J. W., Koech, H. K., Ratemo, C. M., & Koskey, J. C. (2014). Heavy metal concentrations in water, sediments and common carp (Cyprinus carpio) fish species from Lake Naivasha, Kenya. Research Journal of Environmental and Earth Sciences, 6(8), 416–423.
Olowoyo, J. O., Mdakane, S. T. R., & Okedeyi, O. O. (2014). Assessing the levels of trace metal from two fish species harvested from treated waste water stored in a manmade lake Pretoria, South Africa. African Journal of Biotechnology, 11(4), 838–842.
Önsoy, B., Filiz, H., Tarkan, A. S., Bilge, G., & Tarkan, A. N. (2011). Occurrence of non-native fishes in a small man-made lake (Lake Ula, Muğla): past, present, future perspectives. Turkish Journal of Fisheries and Aquatic Sciences, 11(2), 209–215.
Orsay, B., & Duman, E. (2005). The investigation of various charesteristic and fishing power of fishing vessel using in Kemaliye, Peri, and Göktepe Region. Fırat Üniversitesi Fen ve Mühendislik Bilimleri Dergisi, 17(1), 121–129. In Turkish with an English abstract.
Orsay, B., & Duman, E. (2008a). A comparative study on the sales amount and fish species marketed in Elazığ fish market between 2001 and 2005 years [sic]. Science and Engineering Journal of Fırat University, 20(4), 439–447. In Turkish with an English abstract.
Orsay, B., & Duman, E. (2008b). The fishing productivity with gill nets in Çemişgezek Region of Keban Dam Lake. Science and Engineering Journal of Fırat University, 20(4), 563–568. In Turkish with an English abstract.
Özdemir, N., Yılmaz, F., Levent Tuna, A., & Demirak, A. (2010). Heavy metal concentrations in fish (Cyprinus carpio and Carassius carassius) sediment and water found in the Geyik Dam Lake, Turkey. Fresenius Environmental Bulletin, 19(5), 798–804.
Ozen, O. A., Yaman, M., Sarsilmaz, M., Songur, A., & Kus, I. (2002). Testicular zinc, copper and iron concentrations in male rats exposed to subacute and subchronic formaldehyde gas inhalation. Journal of Trace Elements in Medicine and Biology, 16(2), 119–122.
Ozkurt, S. (2000). Boron accumulation in carp tissues (Cyprinus carpio L., 1758) in dam lakes Çötören and Kunduzlar (Kırka-Eskisehir). Turkish Journal of Biology, 24(3), 663–676. In Turkish with an English abstract.
Özmen, M., Güngördü, A., Kucukbay, F. Z., & Güler, R. E. (2006). Monitoring the effects of water pollution on Cyprinus carpio in Karakaya Dam Lake, Turkey. Ecotoxicology, 15(2), 157–169.
Özparlak, H., Arslan, G., & Arslan, E. (2012). Determination of some metal levels in muscle tissue of nine fish species from the Beyşehir Lake. Turkish Journal of Fisheries and Aquatic Sciences, 12(4), 761–770.
Oztürk, M., Bat, L., & Oztürk, M. (1995). The heavy metal levels in different organs and tissues of carp Cyprinus carpio L. 1758, living in Altınkaya dam lake, Samsun (pp. 650–666). Ankara: II Ulusal Ekoloji ve Çevre Kongresi, 11–13 Eylül.
Öztürk, M., Özözen, G., Minareci, O., & Minareci, E. (2008). Determination of heavy metals in fish, water and sediments from the Demirköprü Dam Lake (Turkey). Journal of Applied Biological Sciences, 2(3), 99–104.
Öztürk, M., Özözen, G., Minareci, O., & Minareci, E. (2009). Determination of heavy metals in fish, water and sediments of Avsar Dam Lake in Turkey. Iranian Journal of Environmental Health Science and Engineering, 6(2), 73–80.
Özuluğ, M., Acıpınar, H., Gaygusuz, Ö., Gürsoy, Ç., & Tarkan, A. S. (2005). Effects of human factor on the fish fauna in a drinking-water resource (Ömerli Dam Lake-Istanbul, Turkey). Research Journal of Agriculture and Biological Sciences, 1(1), 50–55.
Ozyurt, C. E., Avsar, D., Ciçek, E., Ozütok, M., & Yeldan, H. (2004). Estimation of the exploitation rate on the carp (Cyprinus carpio Linnaeus, 1758) and pike-perch (Sander lucioperca Linnaeus, 1758) inhabiting in Seyhan Dam Lake. Ege University Journal of Fisheries & Aquatic Sciences, 21(1–2), 79–84. In Turkish with an abstract in English.
Panahandeh, M., Mansouri, N., Khorasani, N., Karbassi, A., & Riazi, B. (2014). A study of heavy metals concentration in water, sediments and Cyprinus carpio, Abramis brama, Carassius carassius species from Anzali wetland. International Journal of Biosciences, 4(11), 51–59.
Patiño, R., Rosen, M. R., Orsak, E. L., Goodbred, S. L., May, T. W., Alvarez, D., Echols, K. R., Wieser, C. W., Ruessler, S., & Torres, L. (2013). Patterns of metal composition and biological condition and their association in male common carp across an environmental contaminant gradient in Lake Mead National Recreation Area, Nevada and Arizona, USA. Science of the Total Environment, 416(1), 215–224.
Patir, B., & Duman, M. (2006). Determination of physicochemical and microbiological changes in smoked mirror carp (Cyprinus carpio L.) fillets during storage. Science and Engineering Journal of Fırat University, 18(2), 189–195. In Turkish with an English abstract.
Pelletier, E. (1995). Environmental organometallic chemistry of mercury, tin, and lead: Present status and perspectives. In A. Tessier & D. R. Turner (Eds.), Metal speciation and bioavailability in aquatic systems (pp. 103–149). New York: Wiley.
Pham, N. T. T., Pulkownik, A., & Buckney, R. T. (2007). Assessment of heavy metals in sediments and aquatic organisms in West Lake (Ho Tay), Hanoi, Vietnam. Lakes & Reservoirs: Research and Management, 12(4), 285–294.
Raeisi, S., Sharifi Rad, J., Sharifi Rad, M., & Zakariaei, H. (2014). Analysis of heavy metals content in water, sediments and fish from the Gorgan bay, southeastern Caspian sea, Iran. International Journal of Advanced Biological and Biomedical Research, 2(6), 2162–2172.
Rowbotham, A. L., Levy, L. S., & Shuker, L. K. (2000). Chromium in the environment: an evaluation of exposure of the UK general population and possible adverse health effects. Journal of Toxicology and Environmental Health, Part B: Critical Reviews, 3(3), 145–178.
Saeedi Saravi, S. S., & Shokrzadeh, M. (2013). Heavy metals contamination in water and three species of most consumed fish sampled from Caspian Sea, 2011. Environmental Monitoring and Assessment, 185(12), 10333–10337.
Sahan, A., Belge Kurutas, E., & Altun, T. (2010). The determination of biochemical indicators (biomarkers) in the common carp (Cyprinus carpio) to the physico-chemical parameters of the Ceyhan River (Adana-Turkey). Ekoloji, 19(76), 8–14.
Sanlı, Y., Demet, O., Akar, F., Yavuz, H., Bilgili, A., Cem Liman, B., & Dogan, A. (1990). Research on natural water quality of Buldan Dam and determination of residual levels of some heavy metals in carp samples obtained from this dam. Ankara Universitesi Veteriner Fakultesi Dergisi, 37(1), 56–73. In Turkish with an English abstract.
Santhi, K., & Prabhahar, C. (2014). Bioaccumulation of heavy metals in the common carp (Cyprinus carpio) in Vellar estuary, Mudasalodai and Muzhukuthurai coastal waters, Tamil Nadu, India. International Journal of Advanced Research in Biological Sciences, 1(7), 193–198.
Saravi, H. N., Pourgholam, R., Pourang, N., Rezaei, M., Makhlough, A., & Unesipour, H. (2013). Heavy metal concentrations in edible tissue of Cyprinus carpio and its target hazard quotients in the Southern Iranian Caspian Sea Coast, (2010). Journal of Mazandaran University of Medical Sciences, 23(103), 32–44. In Persian with an English abstract.
Scherz, H., & Kirchhoff, E. (2006). Trace elements in foods: zinc contents of raw foods—a comparison of data originating from different geographical regions of the world. Journal of Food Composition and Analysis, 19(5), 420–433.
Schiavino, D., Nucera, E., Alonzi, C., Buonomo, A., Pollastrini, E., Roncallo, C., De Pasquale, T., Lombardo, C., La Torre, G., Sabato, V., Pecora, V., & Patriarca, G. (2006). A clinical trial of oral hyposensitization in systemic allergy to nickel. International Journal of Immunopathology & Pharmacology, 19(3), 593–600.
Schmitt, C. J., Brumbaugh, W. G., Linder, G. L., & Hinck, J. E. (2006). A screening-level assessment of lead, cadmium, and zinc in fish and crayfish from Northeastern Oklahoma, USA. Environmental Geochemistry and Health, 28(5), 445–471.
Sevcikova, M., Modra, H., Kruzikova, K., Zitka, O., Hynek, D., Adam, V., Celechovska, O., Kizek, R., & Svobodova, Z. (2013). Effect of metals on metallothionein content in fish from Skalka and Želivka Reservoirs. International Journal of Electrochemical Science, 8(2), 1650–1663.
Short, T. M., DeWeese, L. R., & Dubrovsky, N. M. (2008). Discrimination of trait-based characteristics by trace element bioaccumulation in riverine fishes. Canadian Journal of Fisheries and Aquatic Sciences, 65(6), 1087–1100.
Shumka, S., Paparisto, A., & Grazhdani, S. (2008). Identification of non-native freshwater fishes in Albania and assessment of their potential threats to the national biological freshawater [sic] diversity. Balwois 2008 Proceedings Paper 040, 1–6.
Sobhanardakani, S., & Jafari, S. M. (2014). Heavy metals contamination in silver, common and grass carp caught from Zarivar Lake, western Iran. European Online Journal of Natural and Social Sciences, 3(2), 344–350.
Sobhanardakani, S., Jafari, S. M., & Hamedan, I. (2014). Investigation of As, Hg, Zn, Pb, Cd and Cu concentrations in muscle tissue of Cyprinus carpio. Journal of Mazandaran University of Medical Sciences, 24(116), 184–195. In Persian with an English abstract.
Sorensen, E. M. B. (1991). Metal poisoning in fish. Boca Raton: CRC Press.
Spehar, R. L., Christensen, G. M., Curtis, C., Lemke, A. E., Norberd, T. J., & Pickering, Q. H. (1998). Effects of pollution on freshwater fish. Water Pollution Control Federation, 54(6), 877–922.
Sreedhara Nayaka, B., Ramakrishna, S., & Delvi, M. (2009). Impact of heavy metals on water, fish (Cyprinus carpio) and sediments from a water tank at Tumkur, India. Oceanological and Hydrobiological Studies, 38(2), 17–28.
Storelli, M. M. (2008). Potential human health risk from metals (Hg, Cd, and Pb) and polychlorinated biphenyls (PCBs) via seafood consumption: estimation of target hazard quotients (THQs) and toxic equivalents (TEQs). Food and Chemical Toxicology, 46(8), 2782–2788.
Subotić, S., Spasić, S., Višnjić-Jeftić, Ž., Hegediš, A., Krpo-Ćetković, J., Mićković, B., Skorić, S., & Lenhardt, M. (2013). Heavy metal and trace element bioaccumulation in target tissues of four edible fish species from the Danube River (Serbia). Ecotoxicology and Environmental Safety, 98(1), 196–202.
Tabatabaie, T., Ghomi, M. R., Amiri, F., & Zamani-ahmadmahmoodi, R. (2011). Comparative study of mercury accumulation in two fish species, (Cyprinus carpio and Sander lucioperca) from Anzali and Gomishan wetlands in the southern coast of the Caspian Sea. Bulletin of Environmental Contamination and Toxicology, 87(6), 674–677.
Tarkan, A. S., Marr, S. M., & Ekmekçi, F. G., 2015. Non-native and translocated freshwater fish. FiSHMED Fishes in Mediterranean Environments, 003, 28 pp.
Tekin-Özan, S., & Aktan, N. (2012). Relationship of heavy metals in water, sediment and tissues with total length, weight and seasons of Cyprinus carpio L., 1758 from Işikli Lake (Turkey). Pakistan Journal of Zoology, 44(5), 1405–1416.
Tekin-Özan, S., & Kir, İ. (2008). Seasonal variations of heavy metals in some organs of carp (Cyprinus carpio L., 1758) from Beyşehir Lake (Turkey). Environmental Monitoring and Assessment, 138(1), 201–206.
TFC (2002). Declaration on determination of maximum levels of determined contaminants in Turkish Food Codex. vol 2002/63, 23.09.2002 edn. Turkish Republic Official Gazette, Ankara, Turkey.
TFC (2011). Declaration on maximum limits of contaminants in food. 29.12.2011 edn. Turkish Republic Official Gazette, Ankara, Turkey.
Tiwari, A., & Dwivedi, A. C. (2014). Assessment of heavy metals bioaccumulation in alien fish species, Cyprinus carpio from the Gomti River, India. European Journal of Experimental Biology, 4(6), 112–117.
Tóth, T., Volmannová, A., Musilová, J., Árvay, J., Tomáš, J., Lazor, P., & Stanovic, R. (2014). Cadmium and mercury translocation intissues of common carp (Cyprinus carpio, L.). Poster presentation, ISEAC 38.
Turkish Statistical Institute. (2014). Su Ürünleri İstatistikleri/Fishery Statistics 2013 (p. 75). Ankara: Turkish Statistical Institute, Printing Division.
Tüzen, M. (2003). Determination of heavy metals in fish samples of the middle Black Sea (Turkey) by graphite furnace atomic absorption spectrometry. Food Chemistry, 80(1), 119–123.
Tyokumbur, E. T., & Okorie, T. (2014). Assessment of arsenic and selenium in Cyprinus carpio from Alaro stream in Ibadan, Nigeria. International Journal of Agricultural Sciences and Natural Resources, 1(4), 72–75.
Uysal, H., Tunçer, S., & Yaramaz, Ö. (1987). Investigation of some heavy metal levels of C. carpio, S. glanis, A. anguilla living in Gölcük and Gölmarmara lakes. Türkiye 8 Ulusal Biyoloji Kongresi, 3–5 Eylul 1986, İzmir, pp. 444–453.
Uysal, K., Özden, Y., Çiçek, A., & Köse, E. (2010). Bioaccumulation ratios of sediment-bound heavy metals of Porsuk and Enne dam lakes (Kütahya/Turkey) to different tissues of common carp (Cyprinus carpio). Istanbul University Journal of Fisheries & Aquatic Sciences, 25(2), 1–10.
Velcheva, I. G. (2006). Zinc content in the organs and tissues of freshwater fish from the Kardjali and Studen Kladenets Dam Lakes in Bulgaria. Turkish Journal of Zoology, 30(1), 1–7.
Vicarova, P., Kleckerova, A., Docekalova, H., & Pelcova, P. (2014). Heavy metals in the common carp (Cyprinus carpion [sic.] L.) from two reservoirs in the Czech Republic. In: O. Polák, Cerkal, R. & Škarpa, P. (Eds), Mendelnet 2014 (pp. 522–525). Mendel University in Brno.
Vilizzi, L. (2012). The common carp, Cyprinus carpio, in the Mediterranean Region: origin, distribution, economic benefits, impacts and management. Fisheries Management and Ecology, 19(2), 93–110.
Vilizzi, L., Tarkan, A. S., & Ekmekçi, F. G. (2013). Stock characteristics and management insights for common carp (Cyprinus carpio) from Anatolia: a review of weight–length relationships and condition factors. Turkish Journal of Fisheries and Aquatic Sciences, 13(4), 759–775.
Vilizzi, L., Ekmekçi, F. G., & Tarkan, A. S. (2014a). Natural diet of common carp (Cyprinus carpio L., 1758) in Anatolia (Turkey): a review. Mediterranean Marine Science, 15(1), 216–218.
Vilizzi, L., Tarkan, A. S., & Ekmekçi, F. G. (2014b). Reproductive biology of common carp (Cyprinus carpio L., 1758) in Anatolia (Turkey): a review. Mediterranean Marine Science, 15(1), 218–222.
Vilizzi, L., Tarkan, A. S., & Ekmekçi, F. G. (2015a). Parasites of the common carp Cyprinus carpio L., 1758 (Teleostei: Cyprinidae) from water bodies of Turkey: updated checklist and review for the 1964–2014 period. Turkish Journal of Zoology, 39(4), 545–554.
Vilizzi, L., Ekmekçi, F. G., Tarkan, A. S., & Jackson, Z. J. (2015b). Growth of common carp Cyprinus carpio in Anatolia (Turkey), and relative to native and invasive areas worldwide. Ecology of Freshwater Fish, 24(2), 165–180.
Waalkes, M. P. (2000). Cadmium carcinogenesis in review. Journal of Inorganic Biochemistry, 79(1–4), 241–244.
Walter, T., Pino, P., Pizarro, F., & Lozoff, B. (1998). Prevention of iron-deficiency anemia: comparison of high-and low-iron formulas in term healthy infants after six months of life. The Journal of Pediatrics, 132(4), 635–640.
Wang, W.-C., & Rainbow, P. S. (2008). Comparative approaches to understand metal bioaccumulation in aquatic animals. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 148(4), 315–323.
Yaman, M. (2006). Comprehensive comparison of trace metal concentrations in cancerous and non-cancerous human tissues. Current Medicinal Chemistry, 13(21), 2513–2525.
Yaman, M., Bal, T., & Yaman, I. H. (2013). Metal levels in Trachurus trachurus and Cyprinus carpio in Turkey. Food Additives & Contaminants, Part B: Surveillance, 6(4), 301–306.
Yanar, Y., & Fenercioğlu, H. (1999). The utilization of carp (Cyprinus carpio) flesh as fish ball. Turkish Journal of Veterinary and Animal Sciences, 23(4), 361–365. In Turkish with an abstract in English.
Yancheva, V., Stoyanova, S., Velcheva, I., Petrova, S., & Georgieva, E. (2014). Metal bioaccumulation in common carp and rudd from the Topolnitsa reservoir, Bulgaria. Archives of Industrial Hygiene and Toxicology, 65(1), 57–66.
Yeşilbudak, B., & Erdem, C. (2013). Bioaccumulation of zinc in kidney tissue of common carp (Cyprinus carpio L. 1758) (pp. 19–24). Cappadocia: Digital Proceeding of the ICOEST 2013.
Yeşilbudak, B., & Erdem, C. (2014). Cadmium accumulation in gill, liver, kidney and muscle tissues of common carp, Cyprinus carpio, and Nile tilapia, Oreochromis niloticus. Bulletin of Environmental Contamination and Toxicology, 92(5), 546–550.
Yousafzai, A. M., Siraj, M., Ahmad, H., & Chivers, D. P. (2012). Bioaccumulation of heavy metals in common carp: implications for human health. Pakistan Journal of Zoology, 44(2), 489–494.
Yousafzai, A. M., Gulfam, N., & Khan, A. (2014). Bioaccumulation of copper (Cu), in water, sediments and in different tissues of Cyprinus carpio, from Kalpani Stream Mardan, Khyber Pakhtunkhwa, Pakistan. The Journal of Zoological Studies, 1(3), 23–30.
Yüngül, M., Harlioğlu, A. G., & Bağcı, E. (2012). Present status of fisheries sector in Elazığ. Türk Bilimsel Derlemeler Dergisi, 5(1), 91–94. In Turkish with an English abstract.
Zengin, M., & Buhan, E. (2007). The evaluation for the change of native fish fauna in Almus-Ataköy Dam Lakes (Yeşilirmak Basin, Tokat,) after fish stocking programme (pp. 267–277). Antalya: Ulusal Su Günleri. In Turkish with an English abstract.
Zhu, F., Qu, L., Fan, W., Wang, A., Hao, H., Li, X., & Yao, S. (2015). Study on heavy metal levels and its health risk assessment in some edible fishes from Nansi Lake, China. Environmental Monitoring and Assessment. doi:10.1007/s10661-015-4355-3.
Zineb, D., & Nacéra, D. Y. (2013). Seasonal variations of some heavy metals in common carp (Cyprinus carpio L., 1758) collected from El Izdihar Dam of Sidi Abdelli (tlemcen) in North-Western Algeria. Annals of Biological Research, 4(1), 232–237.
Zubcov, E., Zubcov, N., Ene, A., & Biletchi, L. (2012). Assessment of copper and zinc levels in fish from freshwater ecosystems of Moldova. Environmental Science and Pollution Research, 19(6), 2238–2247.
Acknowledgments
The authors are grateful to to Güler Ekmekçi, Baran Yoğurtçuoğlu, Fatma Kübra Erbay, Cüneyt Solak, Ünal Erdem, Naime Arslan, Ruşen Ustaoğlu, Oğuz Öztürk and İbrahim Cengizler for assistance with literature retrieval and organisation. Contribution to this study by LV was through a 2221 Fellowship Programme granted by The Scientific & Technological Research Council of Turkey (TÜBİTAK) and The Department of Science Fellowships & Grant Programs (BİDEB).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Vilizzi, L., Tarkan, A.S. Bioaccumulation of metals in common carp (Cyprinus carpio L.) from water bodies of Anatolia (Turkey): a review with implications for fisheries and human food consumption. Environ Monit Assess 188, 243 (2016). https://doi.org/10.1007/s10661-016-5248-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-016-5248-9