Bioaccumulative and conchological assessment of heavy metal transfer in a soil-plant-snail food chain

Springer Science and Business Media LLC - 2012
Dragoş Nica1, Marian Bura1, I. Gergen2, Monica Hărmănescu3, Despina-Maria Bordean2
1Banat's University of Agricultural Sciences and Veterinary Medicine from Timisoara, Faculty of Animal Sciences and Biotechnologies, Timisoara, Calea Aradului 119, RO, 300645, Romania
2Banat's University of Agricultural Sciences and Veterinary Medicine from Timisoara, Faculty of Food Processing Technology, Calea Aradului 119, RO, 300645, Timisoara, Romania
3Banat’s University of Agricultural Sciences and Veterinary Medicine from Timisoara, Faculty of Agriculture, Timisoara, RO, 300645, Calea Aradului 119, Romania

Tóm tắt

Abstract Background Copper (Cu), zinc (Zn), cadmium (Cd), and lead (Pb) can pose serious threats to environmental health because they tend to bioaccumulate in terrestrial ecosystems. We investigated under field conditions the transfer of these heavy metals in a soil-plant-snail food chain in Banat area, Romania. The main goal of this paper was to assess the Roman snail (Helix pomatia) usefulness in environmental monitoring as bioindicator of heavy metal accumulation. Eight sampling sites, selected by different history of heavy metal (HM) exposure, were chosen to be sampled for soil, nettle leaves, and newly matured snails. This study also aimed to identify the putative effects of HM accumulation in the environment on phenotypic variability in selected shell features, which included shell height (SH), relative shell height (RSH), and whorl number (WN). Results Significantly higher amounts of HMs were accumulated in snail hepatopancreas and not in foot. Cu, Zn, and Cd have biomagnified in the snail body, particularly in the hepatopancreas. In contrast, Pb decreased when going up into the food chain. Zn, Cd, and Pb correlated highly with each other at all levels of the investigated food chain. Zn and Pb exhibited an effective soil–plant transfer, whereas in the snail body only foot Cu concentration was correlated with that in soil. There were significant differences among sampling sites for WN, SH, and RSH when compared with reference snails. WN was strongly correlated with Cd and Pb concentrations in nettle leaves but not with Cu and Zn. SH was independent of HM concentrations in soil, snail hepatopancreas, and foot. However, SH correlated negatively with nettle leaves concentrations for each HM except Cu. In contrast, RSH correlated significantly only with Pb concentration in hepatopancreas. Conclusions The snail hepatopancreas accumulates high amounts of HMs, and therefore, this organ can function as a reliable biomarker for tracking HM bioavailability in soil. Long-term exposure to HMs via contaminated food might influence the variability of shell traits in snail populations. Therefore, our results highlight the Roman snail (Helix pomatia) potential to be used in environmental monitoring studies as bioindicator of HM pollution.

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Tài liệu tham khảo

Lovett GM, Burns DA, Driscoll CT, Jenkins JC, Mitchell MJ, Rustad L, Shanley JE, Likens GE, Haeuber R: Who needs environmental monitoring?. Front Ecol Environ. 2007, 5: 253-260. 10.1890/1540-9295(2007)5[253:WNEM]2.0.CO;2.

Wharfe J: Hazardous chemicals in complex mixtures – a role for direct toxicity assessment. Ecotoxicology. 2004, 13: 81-88.

Murariu M, Dragan ES, Drochioiu G: Electrospray ionization mass spectrometric approach of conformationally-induced metal binding to oligopeptides. Eur J Mass Spectrom. 2010, 16: 511-521. 10.1255/ejms.1092.

Sillins I, Hogberg J: Combined toxic exposures and human health: biomarkers of exposure and effect. Int J Environ Res Public Health. 2011, 8: 629-647. 10.3390/ijerph8030629.

Agarwal SK: Heavy metal pollution. 2009, New Delhi: APH Publishing Corporation, 1-89.

Ryu H, Chung JS, Nam T, Moon HS, Nam K: Incorporation of heavy metals bioavailability into risk characterization. Clean. 2010, 38: 812-815.

Tomasik P, Magadza CM, Mhinz AS, Chirume A, Zaranyika MF, Muchiriri S: The metal-metal interaction in biological systems. Part IV. Freshwater snail Bulinus globosus. Water Air Soil Pollut. 1995, 83: 123-145. 10.1007/BF00482599.

Ren S, Mee RW, Frymier PD: Using factorial experiments to study the toxicity of metal mixtures. Ecotoxicol Environ Saf. 2004, 59: 38-43. 10.1016/S0147-6513(03)00099-X.

Maynard R: Key airborne pollutants - the impact on health. Sci Total Environ. 2004, 334–335: 9-13.

MWFEP(Romania Ministry of Waters, Forests and Environmental Protection): Ordinul nr. 756/1997 al Ministerului Apelor, Padurilor şi Protecţiei Mediului pentru aprobarea Reglementării privind evaluarea poluarii mediului modificat de Ordinul nr. 1144, [http://www.unimed.ro/Ordin%20nr.%201144-2002.pdf], /2002 al Ministerului Apelor şi Protecţei Mediului,

Moigradean D, Lazureanu A, Poiana MA, Harmanescu M, Gogoasa I, Gergen I: The influence of mineral fertilization about nitrogen content in soil, plant and tomato fruit. Bull Univ Agric Sci Vet Med Cluj-Napoca Horti. 2008, 65: 172-177.

Schlosser G, Stefanescu R, Przybylski M, Murariu M, Hudecz F, Drochioiu G: Copper-induced oligomerization of peptides: a model study. Eur J Mass Spectrom. 2007, 13 (5): 331-337.

Peralta JR, Gardea-Torresdey JL, Tiemann KJ, Gomez E, Arteaga S, Rascon E, Parsons JG: Uptake and effects of five heavy metals on seed germination and plant growth in Alfalfa(Medicago sativa L.). Environ Contam Toxicol. 2001, 66: 727-734.

Emsley J: Nature's building blocks: an A-Z guide to the elements. 2001, Oxford: Oxford University Press

Nordberg GF, Sanstrom B, Becking G, Goyer RA: Esentiality and toxicity of metals. Heavy metals in the environment. Edited by: Sarkar B. 2002, New York: Marcel Decker, Inc, 1-31.

Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Morel FMM: A cadmium enzyme from a marine diatom. Nature. 2005, 435: 42-44.

Hillinger N, Olaru M, Turnock D: The role of industrial archaeology in conservation: the Reşiţa area of the Romanian Carpathians. GeoJournal. 2003, 55: 607-630.

Harmanescu M, Alda L, Bordean D, Gogoasa I, Gergen I: Heavy metals health risk assessment for population via consumption of vegetables grown in old mining area; a case study: Banat County, Romania. Chem Cent J. 2011, 5: 64-10.1186/1752-153X-5-64.

Bordean D-M, Gergen I, Pîrvu D, Gogoasa I, Pirvulescu L: Studies concerning heavy metal pollution in Banat area. Bul USAMV-CN. 2006, 62:

Laskowski R, Hopkin SP: Accumulation of Zn, Cu, Pb and Cd in the garden snail (Helix aspersa): implications for predators. Environ Pollut. 1996, 91: 289-297. 10.1016/0269-7491(95)00070-4.

Beeby A, Richmond L: Do the soft tissues of Helix aspersa serve as a quantitative sentinel of predicted free lead concentrations in soil?. Appl Soil Ecol. 2003, 22: 159-165. 10.1016/S0929-1393(02)00130-0.

Notten MJ, Oosthoek AJ, Rozema J, Aerts R: Heavy metal concentrations in a soil-plant-snail food chain along a terrestrial soil pollution gradient. Environ Pollut. 2005, 138: 178-190. 10.1016/j.envpol.2005.01.011.

Dallinger R, Chabicovsky M, Hodl E, Prem C, Hunziker P, Manzl C: Copper in Helix pomatia(Gastropoda) is regulated by one single cell type: differently responsive metal pools in rhogocytes. Am J Physiol Regul Integr Comp Physiol. 2005, 289: R1185-R1195. 10.1152/ajpregu.00052.2005.

Mulvey M, Newman MC, Beeby AN: Genetic and conchological comparison of snails (Helix aspersa) differing in shell deposition of lead. J Molluscan Stud. 1996, 62: 213-223. 10.1093/mollus/62.2.213.

Beeby A, Richmond L, Herpe F: Lead reduces shell mass in juvenile garden snails (Helix aspersa). Environ Pollut. 2002, 120: 283-288. 10.1016/S0269-7491(02)00151-3.

Jordaens K, De Wolf H, Vandecasteele B, Blust R, Backeljau T: Associations between shell strength, shell morphology and heavy metals in the land snail Cepaea nemoralis (Gastropoda, Helicidae). Sci Total Environ. 2006, 363: 285-293. 10.1016/j.scitotenv.2005.12.002.

Viard B, Pihan F, Promeyrat S, Pihan J-C: Integrated assessment of heavy metal (Pb, Zn, Cd) highway pollution: bioaccumulation in soil, Graminaceae and land snails. Chemosphere. 2004, 55: 1349-1359. 10.1016/j.chemosphere.2004.01.003.

Gomot de Vaufleury A: Standardized growth toxicity testing (Cu, Zn, Pb, and Pentachloro phenol) with Helix aspersa. Ecotoxicol Environ Saf. 2000, 46: 41-50. 10.1006/eesa.1999.1872.

Nemes N, Nemes N, Constantinescu L: Geogen pollution with heavy metals in Bistra area, Caras-Severin county. RJAS. 2007, 2: 69-73.

Gogoasa I, Gergen I, Oprea G, Bordean D, Alda L, Moigradean D, Rada M, Bragea M: Preliminary research concerning the distribution of copper in the soil and vegetables in historical anthropic pollution(Caras-Severin County, Romania). J Agroaliment Process Technol. 2011, 17: 371-374.

Gheoca V, Gheoca D: The accumulation of heavy metals in the tissues of Helix pomatia from locations with industrial and town pollution. Transylvanian Rev Syst Ecol Res. 2005, 2: 67-74.

Hobbelen PHF, Koolhaas JC, Van Gestel CAM: Risk assessment of heavy metal pollution for detritivores in floodplain soils in the Biesbosch, The Netherlands, taking bioavailability into account. Environ Pollut. 2004, 129: 409-419. 10.1016/j.envpol.2003.11.010.

Suciu I, Cosma C, Todica M, Bolboaca SD, Jantschi L: Analysis of soil heavy metal pollution and pattern in Central Transylvania. Int J Mol Sci. 2008, 9 (4): 434-453. 10.3390/ijms9040434.

Bordean D-M, Dragomirescu M, Nicula M, Butnariu M, Goian I, Gergen I: Study of lead and cadmium content in soil, water and plants in Freidorf areea. Lucrări Stiintifice: Zootehnie si Biotehnologii. 2004, 37: 37-40.

Kabata-Pendias A: Soil-plant transfer of trace elements: an environmental issue. Geoderma. 2004, 122: 143-149. 10.1016/j.geoderma.2004.01.004.

Ianos G: Conclusions concerning the source and the environment concentration with heavy metals on the etno-historical Banat. Metal Elements in Environment, Medicine and Biology 2008. Tome VIII. 2end edition. Edited by: Silaghi-Dumitrescu I, Garban Z, Dragan P. 2008, Timisoara: Publishing House “Eurobit”, 205-223.

Dallinger R, Berger B, Triebskorn-Kohler R, Kohler H: Soil biology and ecotoxicology. The biology of terrestrial molluscs. Edited by: Barker GM. 2001, Wallingford: CABI Publishing, 489-525.

Rabitsch WB: Metal accumulation in terrestrial pulmonates at a lead/zinc smelter site in Arnoldstein, Austria. Bull Environ Contam Toxicol. 1996, 56: 734-741. 10.1007/s001289900108.

Menta C, Parisi V: Metal concentrations in Helix pomatia, Helix aspersa and Arion rufus: a comparative study. Environ Pollut. 2001, 115: 205-208. 10.1016/S0269-7491(01)00110-5.

Gomot de Vaufleury A, Coeurdassier M, Pandard P, Scheifler R, Lovy C, Crini N, Badot PM: How terrestrial snails can be used in risk assessment of soils. Environ Toxicol Chem. 2006, 25: 797-806. 10.1897/04-560R.1.

Moser H, Wieser W: Copper and nutrition in Helix pomatia (L.). Oecologia. 1979, 42: 241-251. 10.1007/BF00344860.

Nica D, Filimon MN, Borozan AB, Vintila D: Can the environment induce intra-variety changes of Helix pomatia conchological features?. An UO Fasc Biol. 2011, 18: 140-145.

Locher R, Baur B: Sperm delivery and egg production of the simultaneously hermaphroditic land snail Arianta arbustorum exposed to an increased sperm competition risk. Invertebr Reprod Dev. 2000, 38: 53-60. 10.1080/07924259.2000.9652436.

Orstan A: A method to measure shell volumes. Triton. 2011, 23: 31-32.

Tryjanowski P, Koralewska-Batura E: Inter-habitat shell morphometric differentiation of the snail Helix lutescens Rossm. (Gastropoda: Pulmonata). Ekológia (Bratislava). 2002, 19: 11-116.

Eeva T, Rainio K, Suominen O: Effects of pollution on land snail abundance, size and diversity as resources for pied flycatcher, Ficedula hypoleuca. Sci Total Environ. 2010, 408 (19): 4165-4169. 10.1016/j.scitotenv.2010.05.028.

Goodfriend GA: Variation in land snail shell form and size and its causes, a review. Syst Zool. 1986, 35: 204-223. 10.2307/2413431.

Chiba S: Morphological divergence as a result of common adaptation to a shared environment in land snails of the genus Hirasea. J Molluscan Stud. 2009, 75: 253-259. 10.1093/mollus/eyp020.

Madec L, Bellido A, Guiller A: Shell shape of the land snail Cornu aspersum in North Africa, unexpected evidence of a phylogeographical splitting. Heredity. 2003, 91: 224-231. 10.1038/sj.hdy.6800301.

Beeby A, Richmond L: Magnesium and the deposition of lead in the shell of three populations of the garden snail Cantareus aspersus. Environ Pollut. 2011, 159: 1667-1672. 10.1016/j.envpol.2011.02.040.

Hopkins SP: In situ biological monitoring of pollution in terrestrial and aquatic ecosystems. Handbook of ecotoxicology Volume 1. Edited by: Calow P. 1993, Blackwell Scientific, 397-427.

Bura M: Cresterea melcilor o activitate profitabila. 2004, Timişoara: Ed. Eurobit

Baur B: Microgeographical variation in shell size of the land snail Chondrina clienta. Biol J Linn Soc. 1988, 37: 137-155.

Grossu AV: Fauna R.P.R., Mollusca Gastropoda Pulmonata. 1955, Bucuresti: Editura Academiei R.P.R

Borza I, Tarau D, Sala F, Tarau F, Iordache M: Quality state of soils from West of Romania and measures for their fertility restoration. RJAS. 2007, 39: 161-166.

Kerney MP, Cameron RAD: A field guide to the land snails of Britain and northwestern Europe. 1979, London: Collins

Statistica 10: http://www.statsoft.com/products/statistica-10-new-features/,

Hammer R, Harper DAT, Ryan PD: Past: paleontological statistics software package for education and data analysis. Palaeontol Electron. 2001, 4 (1): 9-http://palaeo-electronica.org/2001_1/past/issue1_01.htm,

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