Skip to main content

Advertisement

SpringerLink
Log in

Potentially toxic elements in invasive fish species Prussian carp (Carassius gibelio) from different freshwater ecosystems and human exposure assessment

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Concentrations of Al, As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Se, Sn, and Zn were detected in the muscle and gills of Prussian carp from three different freshwater ecosystems: isolated ponds and the South Morava River in Serbia, and Kopačko Lake in complex wetland ecosystem of the Kopački Rit Nature Reserve in Croatia. The main goals of the present research were to assess the concentrations of potentially toxic elements (PTEs) in the muscle and gills of Prussian carp (Carassius gibelio), to examine whether abiotic factors from three different freshwater ecosystems affect the accumulation of PTEs in fish tissues, and to estimate the human health risk resulting from fish consumption. There were only six concentrations of PTEs in the gill tissue (Cr, Hg, Mn, Pb, Sn, and Zn) that were not significantly different among the different freshwater ecosystems. In the muscles, the differences were much less visible. Kopačko Lake distinguished with the highest values of metal pollution index (MPI) for muscles (0.24) and isolated ponds with the highest values of MPI for gills (0.8). The redundancy analysis (RDA) showed that concentrations of Al, Mn, Zn, Cu, and Fe in the gill tissue were significantly correlated with the environmental variables. In contrast, the RDA based on element concentrations in the fish muscles indicated no significant relationship with the environment. Isolated ponds, with no inflow of freshwater, stand out as the most polluted, followed by Kopačko Lake with occasional floods. Flowing freshwater ecosystem South Morava River can be single out as at least polluted with PTEs. The target hazard quotients (THQ) and hazard index (HI) suggested there were no significant noncarcinogenic health risks. The target carcinogenic risk factor (TR) for As and Pb confirmed there were no cancer risks related to human fish consumption. Since the elevated concentrations of toxic Cd and As in Prussian carp were estimated, an early warning should be assumed, especially for fishing activities in these areas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article (and its supplementary information files).

References

  • Andreji J, Stránai I, Massányi P, Valent M (2006) Accumulation of some metals in muscles of five fish species from lower Nitra river. J Environ Sci Health, Part A 41(11):2607–2622. https://doi.org/10.1080/10934520600928003

    Article  CAS  Google Scholar 

  • APHA (1999) Standard methods for the examination of water and wastewater, 9th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Arumugam A, Li J, Krishnamurthy P, Jia ZX, Leng Z, Ramasamy N, Du D (2020) Investigation of toxic elements in Carassius gibelio and Sinanodonta woodiana and its health risk to humans. Environ Sci Pollut Res 27(16):19955–19969. https://doi.org/10.1007/s11356-020-08554-1

    Article  CAS  Google Scholar 

  • ATSDR-Agency for Toxic Substances and Disease Registry (1998) Toxicological profile for arsenic. Department of Health and Human. Services, Public Health Service, Atlanta, GA, U.S

    Google Scholar 

  • Balik I, Özkök R, Çubuk H, Uysal R (2004) Investigation of some biological characteristics of the silver Crucian Carp, Carassius gibelio (Bloch 1782) Population in Lake Eğirdir. Turk J Zool 28:19–28

    Google Scholar 

  • Bervoets L, Blust R (2003) Metal concentrations in water, sediment, and gudgeon (Gobio gobio) from a pollution gradient: relationship with the fish condition factor. Environ Pollut 126:9–19. https://doi.org/10.1016/S0269-7491(03)00173-8

    Article  CAS  Google Scholar 

  • Bury NR, Walker PA, Glover CN (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206:11–23. https://doi.org/10.1242/jeb.00068

    Article  CAS  Google Scholar 

  • Castro-González MI, Méndez-Armenta M (2008) Heavy metals: implications associated to fish consumption. Environ Toxicol Phar 26:263–271. https://doi.org/10.1016/j.etap.2008.06.001

    Article  CAS  Google Scholar 

  • Chai M, Li R, Tam NFY, Zan Q (2019) Effects of mangrove plant species on accumulation of heavy metals in sediment in a heavily polluted mangrove swamp in Pearl River Estuary, China. Environ Geochem Helth 41:175–189. https://doi.org/10.1007/s10653-018-0107-y

    Article  CAS  Google Scholar 

  • Chien LC, Hung TC, Choang KY, Yeh CY, Meng PJ, Shieh MJ, Han BC (2002) Daily intake of TBT, Cu, Zn, Cd and As for fishermen in Taiwan. Sci Total Environ 285(1–3):177–185. https://doi.org/10.1016/S0048-9697(01)00916-0

    Article  CAS  Google Scholar 

  • Chintala R, Schumacher TE, McDonald LM, Clay DE, Malo DD, Clay SA, Papiernik SK, Julson JL (2013) Phosphorus sorption and availability in biochars and soil biochar mixtures. Clean - Soil Air Water 41(9999):1–9. https://doi.org/10.1002/clen.201300089

    Article  CAS  Google Scholar 

  • Copat C, Bella F, Castaing M, Fallico R, Sciacca S, Ferrante M (2012) Heavy metals concentrations in fish from Sicily (Mediterranean Sea) and evaluation of possible health risks to consumers. B Environ Contam Tox 88:78–83. https://doi.org/10.1007/s00128-011-0433-6

    Article  CAS  Google Scholar 

  • Dallinger R, Kautzky H (1985) The importance of contaminated food and uptake of heavy metals by rainbow trout (Salmo gairdneri): a field study. Oecologia 67:82–89. https://doi.org/10.1007/BF00378455

    Article  Google Scholar 

  • Davutluoglu OI, Seckin G, Ersu CB, Ylmaz T, Sari B (2011) Heavy metal content and distribution in surface sediments of the Seyhan River, Turkey. J Environ Manage 92:2250–2259. https://doi.org/10.1016/j.jenvman.2011.04.013

    Article  CAS  Google Scholar 

  • De Boeck G, Meeus W, Coen WD, Blust R (2004) Tissue-specific Cu bioaccumulation patterns and differences in sensitivity to waterborne Cu in three freshwater fish: rainbow trout (Oncorhynchus mykiss), common carp (Cyprinus carpio), and gibel carp (Carassius auratus gibelio). Aquat Toxicol 70(3):179–188. https://doi.org/10.1016/j.aquatox.2004.07.001

    Article  CAS  Google Scholar 

  • Declerck S, De Bie T, Ercken D, Hampel H, Schrijvers S, Van Wichelen J, Gillard V, Mandiki R, Losson B, Bauwens D, Keijers S, Vyverman W, Goddeeris B, De Meester L, Brendonck L, Mertens K (2006) Ecological characteristics of small farmland ponds: associations with land use practices at multiple spatial scales. Biol Conserv 131:523–532. https://doi.org/10.1016/j.biocon.2006.02.024

    Article  Google Scholar 

  • Đikanović V, Skorić S, Gačić Z (2016) Concentrations of metals and trace elements in different tissues of nine fish species from the Međuvršje Reservoir (West Morava River Basin, Serbia). Arch Biol Sci 68(4):811–819. https://doi.org/10.2298/ABS151104069D

    Article  Google Scholar 

  • Djikanović V, Skorić S, Jarić I, Lenhardt M (2016) Age-specific metal and accumulation patterns in different tissues of nase (Chodrostoma nasus) from the Medjuvršje Reservoir. Sci Total Environ 566:185–190. https://doi.org/10.1016/j.scitotenv.2016.05.072

    Article  CAS  Google Scholar 

  • Downing JA, Prairei JT, Cole JJ, Duarte CM, Tranvik LJ, Striegl RG, Mcdowell H, Kortelainen P, Caraco NF, Melack JM, Middelburg J (2006) The global abundance and size distribution of lakes, ponds, and impoundments. Limnol Oceanogr 51:2388–2397

    Article  Google Scholar 

  • Dragun Z, Krasnići N, Ivanković D, Filipović Marijić V, Mijošek T, Redžović Z, Erk M (2020) Comparison of intracellular trace element distributions in the liver and gills of the invasive freshwater fish species, Prussian carp (Carassius gibelio Bloch, 1782). Sci Total Environ 730:138923. https://doi.org/10.1016/j.scitotenv.2020.138923

    Article  CAS  Google Scholar 

  • European Commission Regulation (2006) Setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union (No 1881/2006)

  • Falfushynska HI, Gnatyshyna LL, Stoliar OB, Nam YK (2011) Various responses to copper and manganese exposure of Carassius auratus gibelio from two populations. Comp Biochem Physiol C: Toxicol Pharmacol 154(3):242–253. https://doi.org/10.1016/j.cbpc.2011.06.001

    Article  CAS  Google Scholar 

  • FAO (1983) Compilation of legal limits for hazardous substances in fish and fishery products. FAO Fish Circ 464:5–100

    Google Scholar 

  • FAO (Food and Agriculture Organization) (2005) National Aquaculture Sector. http://www.fao.org/fishery/countrysector/en/. Accessed 04 Oct 2018)

  • FAO WHO (1989) National Research Council Recommended Dietary Allowances 10 National Academy Press Washington, DC

  • Farkas A, Salánki J, Specziár A (2003) Age- and size specific patterns of heavy metals in the organs of freshwater fish Abramis brama L. populating a low-contaminated site. Water Res 37 (5):959–964

  • Froese R (2006) Cube law, condition factor and weight-length relationships: history, meta-analysis, and recommendations. J Appl Ichthyol 22:241–253. https://doi.org/10.1111/j.1439-0426.2006.00805.x

    Article  Google Scholar 

  • Ghosh L, Adhikari S (2006) Accumulation of heavy metals in freshwater fish—an assessment of toxic interactions with calcium. Am J Food Techol 1(2):139–148

    Article  CAS  Google Scholar 

  • Gómez-Gutiérrez AI, Jover E, Bodineau L, Albaigés J, Bayona JM (2006) Organic contaminant loads into the Western Mediterranean Sea: estimate of Ebro River inputs. Chemosphere 65:224–236. https://doi.org/10.1016/j.chemosphere.2006.02.058

    Article  CAS  Google Scholar 

  • Goyer RA (1997) Toxic and essential metals interactions. Annu Rev Nutr 17:37–50. https://doi.org/10.1146/annurev.nutr.17.1.37

    Article  CAS  Google Scholar 

  • Has-Schön E, Bogut I, Rajković V, Bogut S, Čačić M, Horvatić J (2008) Heavy metal distribution in tissues of six fish species included in human diet, inhabiting freshwaters of the nature park “Hutovo Blato” (Bosnia and Herzegovina). Arch Environ Con Tox 54:75–83. https://doi.org/10.1007/s00244-007-9008-2

    Article  CAS  Google Scholar 

  • 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 (Silurus glanis) from the Buško Blato reservoir (Bosnia and Herzegovina). Chemosphere 135:289–296. https://doi.org/10.1016/j.chemosphere.2015.04.015

    Article  CAS  Google Scholar 

  • Islam MS, Ahmed MK, Habibullah-Al-Mamun M, Islam KN, Ibrahim M, Masunaga S (2014) Arsenic and lead in foods: a potential threat to human health in Bangladesh. Food Addit Contam A 31(12):1982–1992. https://doi.org/10.1080/19440049.2014.9746-86

    Article  CAS  Google Scholar 

  • Jovanović J, Kolarević S, Milošković A, Radojković N, Simić V, Dojčinović B, Kračun-Kolarević M, Paunović M, Kostić J, Sunjog K, Timilijić J, Djordjević J, Gačić Z, Žegura B, Vuković-Gačić B (2018) Evaluation of genotoxic potential in the Velika Morava River Basin in vitro and in situ. Sci Total Environ 621:1289–1299. https://doi.org/10.1016/j.scitotenv.2017.10.099

    Article  CAS  Google Scholar 

  • Kamunde CN, Grosell M, Higgs D, Wood CM (2002) Copper metabolism in actively growing rainbow trout (Oncorhynchus mykiss): interactions between dietary and waterborne copper uptake. J Exp Biol 205:279–290

    Article  CAS  Google Scholar 

  • Klavins M, Briede A, Rodinov V, Kokorite I, Parele E, Klavina I (2000) Heavy metals in rivers of Latvia. Sci Total Environ 262:175–183. https://doi.org/10.1016/S0048-9697(00)00597-0

    Article  CAS  Google Scholar 

  • Klavins M, Potapovics O, Rodinov V (2009) Heavy metals in fish from lakes in Latvia: concentrations and trends of changes. B Environ Contam Tox 82(1):96–100. https://doi.org/10.1007/s00128-008-9510-x

    Article  CAS  Google Scholar 

  • Kristensen P, Globevnik L (2014) European small water bodies. Biology and Environment: Proceeding of the Royal Irish Academy. https://doi.org/10.3318/BIOE.2014.13

  • Laflamme JS, Couillard Y, Campbell GC, Hontela A (2000) Inter renal metallothionein and cortisol secretion in relation to Cd, Cu, and Zn exposure in yellow perch, Perca flavescens, from Abitibi lakes. Can J Fish Aquat Sci 57:1692–1700. https://doi.org/10.1139/f00-118

    Article  CAS  Google Scholar 

  • Mijošek T, Filipović Marijić V, Dragun Z, Ivanković D, Krasnići N, Redžović S, Erk M (2021) Intestine of invasive fish Prussian carp as a target organ in metal exposure assessment of the wastewater impacted freshwater ecosystem. Ecol Indic 122:107247. https://doi.org/10.1016/j.ecolind.2020.107247

    Article  CAS  Google Scholar 

  • Milošković A, Branković S, Simič V, Kovačević S, Ćirković M, Manojlović D (2013) The accumulation and distribution of metals in water, sediment, aquatic macrophytes and fishes of the Gruža Reservoir, Serbia. B Environ Contam Tox 90(5):563–569. https://doi.org/10.1007/s00128-013-0969-8

    Article  CAS  Google Scholar 

  • Milošković A, Simić V (2015) Arsenic and other trace elements in five edible fish species in relation to fish size and weight and potential health risks for human consumption. Pol. J. Environ. Stud. 24:199–206. https://doi.org/10.15244/pjoes/24929

  • Milošković A, Dojčinović B, Kovačević S, Radojković N, Radenković M, Milošević Dj, Simić V (2016) Spatial monitoring of heavy metals in the inland waters of Serbia: a multispecies approach based on commercial fish. Environ Sci Pollut R 23(10):9918–9933. https://doi.org/10.1007/s11356-016-6207-2

    Article  CAS  Google Scholar 

  • Milošković A, Milošević Đ, Radojković N, Radenković M, Đuretanović S, Veličković T, Simić V (2018) Potentially toxic elements in freshwater (Alburnus spp.) and marine (Sardina pilchardus) sardines from the Western Balkan Peninsula: an assessment of human health risk and management. Sci Total Environ 644:899–906. https://doi.org/10.1016/j.scitotenv.2018.07.041

    Article  CAS  Google Scholar 

  • Murtala BA, Abdul WO, Akinyemi AA (2012) Bioaccumulation of heavy metals in fish (Hydrocynus forskahlii, Hyperopisus bebe occidentalis and Clarias gariepinus) organs in downstream Ogun coastal water. Nigeria J Agr Sci 4(11):51–59. https://doi.org/10.5539/jas.v4n11p51

    Article  Google Scholar 

  • Nikolić D, Skorić S, Lenhardt M, Hegediš A, Krpo-Ćetković J (2019) Risk assessment of using fish from different types of reservoirs as human food — a study on European perch (Perca fluviatilis). Environ Pollut 257:113586. https://doi.org/10.1016/j.envpol.2019.113586

    Article  CAS  Google Scholar 

  • Nikolić D, Skorić S, Poleksić V, Rašković B (2021) Sex-specific elemental accumulation and histopathology of pikeperch (Sander lucioperca) from Garaši reservoir (Serbia) with human health risk assessment. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-021-14526-w

  • Petrinec B, Poje Sovilj M, Babić D, Meštrović T, Miklavčić I, Radolić V, Stanić D, Vuković B, Šoštarić M (2018) Assessing the radiological load on the environment in the middle Danube River basin on the basis of a study of the Kopački Rit Nature Park, Croatia. Radiat Environ Biophys 57:285–292. https://doi.org/10.1007/s00411-018-0747-4

    Article  CAS  Google Scholar 

  • Prosi F (1981) Heavy metals in aquatic organisms. In: Förstner U, Wittmann GTW (eds) Berlin. Springer, Heidelberg, New York, pp 271–323. https://doi.org/10.1007/978-3-642-69385-4_6

  • R Core Team. R: A Language and environment for statistical computing; R Foundation for Statistical Computing: Vienna, Austria, 2018. Available online: https://www.r-project.org/ (accessed on 2 July 2018)

  • Radić S, Gregorović G, Stipaničev D, Cvjetko P, Šrut M, Vujčić V, Oreščanin V, Klobučar GIV (2013) Assessment of surface water in the vicinity of fertilizer factory using fish and plants. Ecotoxicol Environ Saf 96:32–40. https://doi.org/10.1016/j.ecoenv.2013.06.023

    Article  CAS  Google Scholar 

  • Rajkowska M, Protasowicki M (2013) Distribution of metals (Fe, Mn, Zn, Cu) in fish tissues in two lakes of different trophy in Northwestern Poland. Environ Monit Assess 185:3493–3502. https://doi.org/10.1007/s10661-012-2805-8

    Article  CAS  Google Scholar 

  • Rajotte JW, Couture P (2002) Effects of environmental metal contamination on the condition, swimming performance, and tissue metabolic capacities of wild yellow perch (Perca flavescens). Can J Fish Aquat Sci 59:1296–1304. https://doi.org/10.1139/F02-095

    Article  CAS  Google Scholar 

  • Rao LM, Padmaja G (2000) Bioaccumulation of heavy metals in M. cyprinoids from the harbor waters of Visakhapatnam. Bulletin Applied Science 192:77–85

    Google Scholar 

  • Rašković B, Poleksić V, Skorić S, Jovičić K, Spasić S, Hegediš A, Vasić N, Lenhardt M (2018) Effects of mine tailing and mixed contamination on metals, trace elements accumulation and histopathology of the chub (Squalius cephalus) tissues: evidence from three differently contaminated sites in Serbia. Ecotox Environ Safe 153:238–247. https://doi.org/10.1016/j.ecoenv.2018.01.058

    Article  CAS  Google Scholar 

  • Reynders H, Bervoets L, Gelders M, De Coen WM, Blust R (2008) Accumulation and effects of metals in caged carp and resident roach along a metal pollution gradient. Sci Total Environ 3911:82–95. https://doi.org/10.1016/j.scitotenv.2007.10.056

    Article  CAS  Google Scholar 

  • Sirot V, Guérin T, Volatier JL, Leblanc JC (2009) Dietary exposure and biomarkers of arsenic in consumers of fish and shellfish from France. Sci Total Environ 407:1875–1885. https://doi.org/10.1016/j.scitotenv.2008.11.050

    Article  CAS  Google Scholar 

  • Skorić S, Višnjić-Jeftić Z, Jarić I, Djikanović V, Mićković B, Nikčević M, Lenhardt M (2012) Accumulation of 20 elements in great cormorant (Phalacrocorax carbo) and its main prey, common carp (Cyprinus carpio) and Prussian carp (Carassius gibelio). Ecotox Environ Safe 80:244–251. https://doi.org/10.1016/j.ecoenv.2012.03.004

    Article  CAS  Google Scholar 

  • Smederevac-Lalić M, Višnjić-Jeftić Ž, Pucar M, Mićković B, Skorić S, Nikčević M, Hegediš A (2011) Fishing circumstances on the Danube in Serbia. Water Res Manag 1(4):45–49

    Google Scholar 

  • Stamenković O, Stojković Piperac M, Milošević Dj, Buzhdygan O, Petrović A, Jenačković D, Ðurđević A, Čerba D, Vlaičević B, Nikolić D, Simić V (2019) Anthropogenic pressure explains variations in the biodiversity of pond communities along environmental gradients: a case study in south-eastern Serbia. Hydrobiologia 838:65–83. https://doi.org/10.1007/s10750-019-03978-4

    Article  CAS  Google Scholar 

  • Storelli MM (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 Chem Toxicol 46:2782–2788. https://doi.org/10.1016/j.fct.2008.05.011

    Article  CAS  Google Scholar 

  • Subotić S, Spasić S, Višnjić-Jeftić Z, Hegediš A, Krpo-Ćetković J, Mićković B, Skorić S, Lenhardt M (2013a) Heavy metal and trace element bioaccumulation in target tissues of four edible fish species from the Danube River (Serbia). Ecotox Environ Safe 98:196–202. https://doi.org/10.1016/j.ecoenv.2013.08.020

    Article  CAS  Google Scholar 

  • Subotić S, Višnjić Jeftić Ž, Spasić S, Hegediš A, Krpo-Ćetković J, Lenhardt M (2013b) Distribution and accumulation of elements (As, Cu, Fe, Hg, Mn, and Zn) in tissues of fish species from different trophic levels in the Danube River at the confluence with the Sava River (Serbia). Environ Sci Pollut Res 20(8):5309–5317. https://doi.org/10.1007/s11356-013-1522-3

    Article  CAS  Google Scholar 

  • Syasina IG, Khlopova AV, Chukhlebova LM (2012) Assessment of the state of the gibel carp Carassius auratus gibelio in the Amur River Basin: heavy-metal and arsenic concentrations and histopathology of internal organs. Arch Environ Con Tox 62(3):465–478. https://doi.org/10.1007/s00244-011-9719-2

    Article  CAS  Google Scholar 

  • Terra BF, Araújo FG, Calza CF, Lopes RT, Teixeira TP (2008) Heavy metal in tissues of three fish species from different trophic levels in a tropical Brazilian river. Water Air Soil Poll 187:275–284. https://doi.org/10.1007/s11270-007-9515-9

    Article  CAS  Google Scholar 

  • US EPA (1997) Mercury study report to Congress health effects of mercury and mercury compounds, vol. V. Washington (DC) 7 United States Environmental Protection agency, EPA-452/ R-97–007

  • US EPA (2000) Risk-based concentration table. Philadelphia PA: United States Environmental Protection Agency, Washington DC

  • Usero J, González-Regalad E, Gracia I (1997) Trace metals in the bivalve mollusks Ruditapes decussates and Ruditapes philippinarum from the Atlantic Coast of Southern Spain. Environ Int 23(3):291–298. https://doi.org/10.1016/S0160-4120(97)00030-5

    Article  CAS  Google Scholar 

  • USFWS (2012) Prussian Carp (Carassius gibelio) Ecological risk screening summary. Web Version e 8/14/2012. U.S. Fish and Wildlife Service. www.fws.gov/injuriouswildlife/pdf_files/Carassius_gibelio_WEB_8-14-2012.pdf. Accessed 3 Jun 2021

  • Uysal K, Köse E, Bülbül M, Dönmez M, Erdoğan Y, Koyun M, Ömeroğlu Ç, Özmal F (2009) The comparison of heavy metal accumulation ratios of some fish species in Enne Dame Lake (Kütahya/Turkey). Environ Monit Assess 157(1–4):355–362. https://doi.org/10.1007/s10661-008-0540-y

    Article  CAS  Google Scholar 

  • Yılmaz AB, Doğan M (2008) Heavy metals in water and in tissues of himri (Carasobarbus luteus) from Orontes (Asi) River, Turkey. Environ Monit Assess 144:437–444. https://doi.org/10.1007/s10661-007-0005-8

    Article  CAS  Google Scholar 

  • Zhelev ZM, Tsonev SV, Boyadziev PS (2018) Significant changes in morphophysiological and haematological parameters of Carassius gibelio (Bloch, 1782) (Actinopterygii: Cyprinidae) as response to sporadic effusions of industrial wastewater into the Sazliyka River, Southern Bulgaria. Acta Zool Bulg 70(4):547–556

    Google Scholar 

  • Zhelyazkov GI, Georgiev DM, Peeva SP, Kalcheva SE, Georgieva KY (2018) Chemical composition and levels of heavy metals in fish meat of the Cyprinidae family from Zhrebchevo Dam, Central Bulgaria. Ecol Balk 10:133–140

    Google Scholar 

  • Zheng N, Wang Q, Zhang X, Zheng D, Zhang Z, Zhang S (2007) Population health risk due to dietary intake of heavy metals in the industrial area of Huludao city. China Sci Total Environ 387(1–3):96–104. https://doi.org/10.1016/j.scitotenv.2007.07.044

    Article  CAS  Google Scholar 

  • Zrnčić S, Oraić D, Ćaleta M, Mihaljević Ž, Zanella D, Bilandžić N (2013) Biomonitoring of heavy metals in fish from the Danube River. Environ Monit Assess 185(2):1189–1198. https://doi.org/10.1007/s10661-012-2625-x

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We want to thank Sonja Dix (UK) for the final English correction.

Funding

The study was supported by a grant (Agreement No 451–03-9/2021–14/200378) and a bilateral cooperation scientific project between Serbia and Croatia, both funded by the Serbian Ministry of Education, Science and Technological Development.

Author information

Authors and Affiliations

  1. Department of Science, Institute for Information Technologies Kragujevac, University of Kragujevac, Jovana Cvijića bb, 34000, Kragujevac, Serbia

    Aleksandra Milošković

  2. Department of Biology and Ecology, Faculty of Sciences and Mathematics, University of Niš, Višegradska 33, 18000, Niš, Serbia

    Milica Stojković Piperac & Đurađ Milošević

  3. Institute of Biology and Ecology, Faculty of Science, University of Kragujevac, Radoja Domanovića 12, 34000, Kragujevac, Serbia

    Nataša Kojadinović, Milena Radenković, Simona Đuretanović & Vladica Simić

  4. Department of Biology, Josip Juraj Strossmayer University of Osijek, Cara Hadrijana 8/A, 31000, Osijek, Croatia

    Dubravka Čerba

Authors
  1. Aleksandra Milošković
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Milica Stojković Piperac
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nataša Kojadinović
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Milena Radenković
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Simona Đuretanović
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dubravka Čerba
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Đurađ Milošević
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Vladica Simić
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: Aleksandra Milošković; Methodology: Aleksandra Milošković, Nataša Kojadinović; Formal analysis and investigation: Milica Stojković Piperac, Dubravka Čerba, Đurađ Milošević, Nataša Radojković; Writing — original draft preparation: Aleksandra Milošković, Milena Radenković, Simona Đuretanović; Supervision: Vladica Simić.

Corresponding author

Correspondence to Aleksandra Milošković.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Bruno Nunes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Milošković, A., Stojković Piperac, M., Kojadinović, N. et al. Potentially toxic elements in invasive fish species Prussian carp (Carassius gibelio) from different freshwater ecosystems and human exposure assessment. Environ Sci Pollut Res 29, 29152–29164 (2022). https://doi.org/10.1007/s11356-021-17865-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-17865-w

Keywords

Search

Navigation