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Seasonal distributions of heavy metal concentrations in different snail (Helix pomatia) tissues from an urban environment in Serbia

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Abstract

The aim of this study was to evaluate the differences between concentrations of heavy metals (cadmium, copper, zinc, iron, and manganese) in terrestrial gastropods, Helix pomatia, collected in four different environment locations in Pančevo city, Serbia. Metal concentrations in the foot and in the digestive gland were measured. Heavy metals cadmium, copper, zinc, iron, and manganese were measured in triplicate by atomic absorption spectrophotometry. Also, this study investigated correlations between the trace element content in the soft tissues and different seasons (summer and fall). The results showed that heavy metal concentrations of the measured elements in both snail tissues were significantly higher in polluted sites when compared to the background levels in the city. In digestive gland tissues, the concentration of heavy metals was higher compared with that in foot tissues. The bioaccumulation (heavy metal concentrations in soft tissues) of heavy metals (Cd, Cu, Zn, Fe, and Mn) in snails, Helix pomatia, has been assessed and related to seasons and sites. Heavy metal accumulation in the soft tissues of snails could provide a powerful monitoring tool for the assessment of environmental heavy metal pollution.

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References

  • Ab Lah R, Smith J, Savins D, Dowell A, Bucher D, Benkendorff K (2017) Investigation of nutritional properties of three species of marine turban snails for human consumption. Food Sci Nutr 5(1):14–30

    Article  CAS  Google Scholar 

  • Ametepey ST, Cobbina SJ, Akpabey FJ, Duwiejuah AB, Abuntori ZN (2018) Health risk assessment and heavy metal contamination levels in vegetables from Tamale Metropolis, Ghana. Int J Food Contam 5(1):5

    Article  Google Scholar 

  • Aprile FM, Bouvy M (2008) Distribution and enrichment of heavy metals at the Tapacurá River basin, northeastern Brazil. Braz J Aquat Sci Technol 12(1):1–8

    Article  CAS  Google Scholar 

  • Bayen S (2012) Occurrence, bioavailability and toxic effects of trace metals and organic contaminants in mangrove ecosystems: a review. Environ Int 48:84–101

    Article  CAS  Google Scholar 

  • Beeby A, Richmond L (2003) Do the soft tissues of Helix aspersa serve as a quantitative sentinel of predicted free lead concentrations in soils? Appl Soil Ecol 22(2):159–165

    Article  Google Scholar 

  • Beeby A, Richmond L, Herpé F (2002) Lead reduces shell mass in juvenile garden snails (Helix aspersa). Environ Pollut 120(2):283–288

    Article  CAS  Google Scholar 

  • Berger B, Dallinger R (1993) Terrestrial snails as quantitative indicators of environmental metal pollution. Environ Monit Assess 25:65–84

    Article  CAS  Google Scholar 

  • Chafik A, Cheggour M, Cossa D, Benbrahim S, Sifeddine M (2001) Quality of Moroccan Atlantic coastal water monitoring and mussel watching. Aquat Living Resour 14:239–249

    Article  Google Scholar 

  • Coeurdassier M, Scheifler R, De Vaufleury A, Crini N, Saccomani C, Du Mont LS, Badot PM (2007) Earthworms influence metal transfer from soil to snails. Appl Soil Ecol 35(2):302–310

    Article  Google Scholar 

  • Dallinger R, Berger B, Hunziger P, Kgi JH (1997) Metallothionein in snail Cd and Cu metabolism. Nature 388(6639):237

    Article  CAS  Google Scholar 

  • Dallinger R, Chabicovsky M, Hodl E, Prem C, Hunziker P, Manzl C (2005) Copper in Helix pomatia (Gastropoda) is regulated by one single cell type: differently responsive metal pools in rhogocytes. Am J Phys Regul Integr Comp Phys 289(4):1185–1195

    Google Scholar 

  • Dragićević O, Baltić MŽ (2005) Snail meat: significance and consumption. Vet Glas 59(3–4):463–474

    Article  Google Scholar 

  • FAO (2015) Fishery statistical collections: global capture production. Food and Agriculture Organization of the United Nations

  • Frontasyeva MV, Galinskaya TY, Krmar M, Matavuly M, Pavlov SS, Povtoreyko EA, Steinnes E (2004) Atmospheric deposition of heavy metals in northern Serbia and Bosnia-Herzegovina studied by the moss biomonitoring, neutron activation analysis and GIS technology. J Radioanal Nucl Chem 259(1):141–144

    Article  CAS  Google Scholar 

  • Gomot A, Pihan F (1997) Comparison of the bioaccumulation capacities of copper and zinc in two snail subspecies (Helix). Ecotoxicol Environ Saf 38(2):85–94

    Article  CAS  Google Scholar 

  • Gomot de Valfleury A, Pihan F (2000) Growing snails used as sentinels to evaluate terrestrial environment contamination by trace element. Chemosphere 40:275–284

    Article  Google Scholar 

  • Gomot de Vaufleury A (2000) Standardized growth toxicity testing (Cu, Zn, Pb, and pentachlorophenol) with Helix aspersa. Ecotoxicol Environ Saf 46(1):41–50

    Article  CAS  Google Scholar 

  • Gu YG, Li QS, Fang JH, He BY, Fu HB, Tong ZJ (2014) Identification of heavy metal sources in the reclaimed farmland soils of the Pearl River estuary in China using a multivariate geostatistical approach. Ecotoxicol Environ Saf 105:7–12

    Article  CAS  Google Scholar 

  • Ivanović J, Janjić J, Baltić M, Milanov R, Bošković M, Marković RV, Glamočlija N (2016) Metal concentrations in water, sediment and three fish species from the Danube River, Serbia: a cause for environmental concern. Environ Sci Pollut Res 23(17):17105–17112

    Article  Google Scholar 

  • Janjić J, Ivanović J, Marković R, Starčević M, Bošković M, Đorđević V, Baltić MŽ (2015) Metal concentration in muscle tissue of carp and pike from different fish ponds in Belgrade area. J Agric Sci Technol 5:429–436

    Google Scholar 

  • Jordaens K, De Wolf H, Vandecasteele B, Blust R, Backeljau T (2006) Associations between shell strength, shell morphology and heavy metals in the land snail Cepaea nemoralis (Gastropoda, Helicidae). Sci Total Environ 363(1–3):285–293

    Article  CAS  Google Scholar 

  • Jovanović DA, Marković RV, Teodorović VB, Šefer DS, Krstić MP, Radulović SB, Baltić MŽ (2017) Determination of heavy metals in muscle tissue of six fish species with different feeding habits from the Danube River, Belgrade—public health and environmental risk assessment. Environ Sci Pollut Res 24(12):11383–11391

    Article  Google Scholar 

  • Langston WJ, Spence SK (1995) Biological factors involved in metal concentrations observed in aquatic organisms. In: Tessier A, Turner DR (eds) Metal speciation and bioavailability in aquatic systems. IUPAC, Wiley, pp 407–478

  • Laskowski R, Hopkin SP (1996) Effect of Zn, Cu, Pb, and Cd on fitness in snails (Helix aspersa). Ecotoxicol Environ Saf 34(1):59–69

    Article  CAS  Google Scholar 

  • Leiva GE, Castilla JC (2002) A review of the world marine gastropod fishery: evolution of catches, management and the Chilean experience. Rev Fish Biol Fish 11(4):283–300

    Article  Google Scholar 

  • Mahaffey KR, Clickner RP, Jeffries RA (2008) Methylmercury and omega-3 fatty acids: co-occurrence of dietary sources with emphasis on fish and shellfish. Environ Res 107:20–29

    Article  CAS  Google Scholar 

  • Massadeh AM, Alomary AA, Mir S, Momani FA, Haddad HI, Hadad YA (2016) Analysis of Zn, Cd, As, Cu, Pb, and Fe in snails as bioindicators and soil samples near traffic road by ICP-OES. Environ Sci Pollut Res 23(13):13424–13431

    Article  CAS  Google Scholar 

  • Melgar C, Geissen V, Cram S, Sokolov M, Bastidas P, Ruiz Suárez LE, Jarquín Sanchez A (2008) Pollutants in drainage channels following long-term application of Mancozeb to banana plantations in southeastern Mexico. J Plant Nutr Soil Sci 171(4):597–604

    Article  CAS  Google Scholar 

  • Mendoza-Carranza M, Sepúlveda-Lozada A, Dias-Ferreira C, Geissen V (2016) Distribution and bioconcentration of heavy metals in a tropical aquatic food web: a case study of a tropical estuarine lagoon in SE Mexico. Environ Pollut 210:155–165

    Article  CAS  Google Scholar 

  • Mikac N, Kwokal Z, Martincic D, Branica M (1996) Uptake of mercury species by transplanted mussels Mytilus galloprovincialis under estuarine conditions (Krka river estuary). Sci Total Environ 184(3):173–182

    Article  CAS  Google Scholar 

  • Milanov ĐR, Krstić PM, Marković VR, Jovanović AD, Baltić MB, Ivanović SJ, Baltić ŽM (2016) Analysis of heavy metals concentration in tissues of three different fish species included in human diet from Danube River. Acta Vet Beograd 66(1):89–102

    Article  Google Scholar 

  • Mooney BD, Nichols PI, Elliot NG (2002) Seafood the good food II: oil profiles for further Australian seafoods and influencing factors. CSIRO Division of Marine Research and Deakin, Hobart A.C.T.: Fisheries Research & Development Corporation (FRDC), Australia

    Google Scholar 

  • Nica DV, Bura M, Gergen I, Harmanescu M, Bordean DM (2012) Bioaccumulative and conchological assessment of heavy metal transfer in a soil-plant-snail food chain. Chem Cent J 6(1):55

    Article  CAS  Google Scholar 

  • Notten MJM, Oosthoek AJP, Rozema J, Aerts R (2005) Heavy metal concentrations in a soil–plant–snail food chain along a terrestrial soil pollution gradient. Environ Pollut 138(1):178–190

    Article  CAS  Google Scholar 

  • Odzak N (2002) Trace metal bioavailability in saline waters, field experiments. CIESM workshop Monogr 19: 37–41

  • Radwan MA, El-Gendy KS, Gad AF (2010) Biomarkers of oxidative stress in the land snail, Theba pisana for assessing ecotoxicological effects of urban metal pollution. Chemosphere 79(1):40–46

    Article  CAS  Google Scholar 

  • Rainbow PS, Phillips DH (1993) Cosmopolitan bio-monitors of trace metals. Mar Poll Bull 26:593–601

    Article  CAS  Google Scholar 

  • Regoli F, Gorbi S, Fattorini D, Tedesco S, Notti A, Machella N, Bocchetti R, Benedetti M, Piva F (2006) Use of the land snail Helix aspersa as sentinel organism for monitoring ecotoxicologic effects of urban pollution: an integrated approach. Environ Health Perspect 114:63–69

    Article  CAS  Google Scholar 

  • Rouane-Hacene O, Boutiba Z, Belhaouari B, Guibbolini-Sabatier ME, Francour P, Risso-de Faverney C (2015) Seasonal assessment of biological indices, bioaccumulation and bioavailability of heavy metals in mussels Mytilus galloprovincialis from Algerian west coast, applied to environmental monitoring. Oceanologia 57(4):362–374

    Article  Google Scholar 

  • Scheifler R, Gomot-de Vaufleury A, Toussaint ML, Badot PM (2002) Transfer and effects of cadmium in an experimental food chain involving the snail Helix aspersa and the predatory carabid beetle Chrysocarabus splendens. Chemosphere 48(6):571–579

    Article  CAS  Google Scholar 

  • Sharaf HM, Shehata AM (2015) Heavy metals and hydrocarbon concentrations in water, sediments and tissue of Cyclope neritea from two sites in Suez Canal, Egypt and histopathological effects. Environ Health Sci Eng 13(1):14

    Article  Google Scholar 

  • Swaileh KM, Rabay'a N, Salim R, Ezzughayyar A, Rabbo AA (2001) Concentrations of heavy metals in roadside soils, plants, and land snails from the West Bank, Palestine. J Environ Sci Health A 36(5):765–778

    Article  CAS  Google Scholar 

  • Viard B, Pihan F, Promeyrat S, Pihan JC (2004) Integrated assessment of heavy metal (Pb, Zn, Cd) highway pollution: bioaccumulation in soil, Graminaceae and land snails. Chemosphere 55(10):1349–1359

    Article  CAS  Google Scholar 

  • Ying W, Ahsanullah M, Batley GE (1993) Accumulation and regulation of heavy metals by the intertidal snail Polinices sordidus. J Mar Biol 116(3):417–422

    Article  CAS  Google Scholar 

Download references

Funding

This paper was supported by the Ministry of Education, Science, and Technological Development, Republic of Serbia, through the funding of the Project: Selected biological hazards to the safety/quality of food of animal origin and the control measures from farm to consumer (31034).

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Authors and Affiliations

  1. Faculty of Veterinary Medicine, University of Belgrade, Bulevar Oslobođenja 18, Belgrade, 11000, Republic of Serbia

    Jelena Ćirić, Radmila Marković, Jelena Janjić & Milan Ž. Baltić

  2. U.S. Food and Drug Administration, 10903 New Hampshire Avenue, Silver Spring, MD, 20993, USA

    Olgica Cerić

  3. Institute of Meat Hygiene and Technology, Kaćanskog 13, Belgrade, 11000, Republic of Serbia

    Danka Spirić & Branislav Baltić

  4. Faculty of Medicine Novi Sad, University of Novi Sad, Serbia and Institute of Public Health of Vojvodina, Novi Sad, Serbia

    Milka Popović

  5. Veterinary Institute of the Republic of Srpska “Dr Vaso Butozan”, Branka Radicevica 18, 78000, Banja Luka, Republic of Srpska

    Biljana Pećanac

Authors
  1. Jelena Ćirić
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  2. Olgica Cerić
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  3. Radmila Marković
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  4. Jelena Janjić
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  5. Danka Spirić
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  6. Milka Popović
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  7. Biljana Pećanac
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  8. Branislav Baltić
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  9. Milan Ž. Baltić
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Correspondence to Jelena Ćirić.

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Responsible editor: Philippe Garrigues

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Ćirić, J., Cerić, O., Marković, R. et al. Seasonal distributions of heavy metal concentrations in different snail (Helix pomatia) tissues from an urban environment in Serbia. Environ Sci Pollut Res 25, 33415–33422 (2018). https://doi.org/10.1007/s11356-018-3295-1

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  • DOI: https://doi.org/10.1007/s11356-018-3295-1

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