Skip to main content
Log in

Field evaluation of metal bioaccumulation in the gastropod Helix aspersa at agricultural and industrial sites in Lebanon

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript


Juvenile Helix aspersa Müller exposed in field microcosms were used to assess the spatial and temporal bioaccumulation of Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn at two agricultural and two industrial sites in Lebanon. The study was performed over a 12-week period where caged snails were sampled once every 3 weeks and assessed for metal bioaccumulation and partitioning between soft tissue and shells. Results showed that metal bioaccumulation by snails was site dependent, with Fe and Cd being the greatest and least accumulated metals, respectively. Significant differences between bioaccumulation in each of the matrices (soft tissue and shells) were also observed. Time-dependent bioaccumulation results showed an increasing accumulation trend at both agricultural sites, while a slight decline was observed at the end of the sampling campaign for the industrial sites. The study of the bioaccumulation factors (BAF) revealed that tested H. aspersa were macroconcentrators for Zn and Cd (BAF > 2) and deconcentrators for all other analyzed elements (BAF < 1). The high partitioning factor values obtained for Cu and Zn indicate an affinity of these two elements for the soft tissues of the snails. The results of this field study indicate that H. aspersa are well suited for active biomonitoring and could provide reliable information on metal pollution and bioavailability.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.


  • Abdel-Halim, K. Y., Abo El-Saad, A. M., Talha, M. M., Hussein, A. A., & Bakry, N. M. (2013). Oxidative stress on land snail Helix aspersa as a sentinel organism for ecotoxicological effects of urban pollution with heavy metals. Chemosphere, 93(6), 1131–1138.

    Article  CAS  Google Scholar 

  • Ali, H., Khan, E., & Ilahi, I. (2019). Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. Journal of chemistry

  • Ali, M. M., Hossain, D., Khan, M. S., Begum, M., & Osman, M. H. (2021). Environmental pollution with heavy metals: a public health concern.

  • ASTM. (2007). Standard test methods for moisture, ash, and organic matter of peat and other organic soils. D2974–07.

  • Bade, R., Oh, S., & Shin, W. S. (2012). Diffusive gradients in thin films (DGT) for the prediction of bioavailability of heavy metals in contaminated soils to earthworm (Eisenia foetida) and oral bioavailable concentrations. Science of The Total Environment, 416, 127–136.

  • Baltaş, H., Şirin, M., Çiloglu, E., Iminova, G., & Çevik, U. (2021). Bio-kinetics of cesium-137 in Mediterranean mussel (Mytilus galloprovincialis) and sea snail (Rapana venosa) via seawater exposure. Journal of Sea Research, 176, 102112.

  • Baroudi, F., Al Alam, J., Fajloun, Z., & Millet, M. (2020). Snail as sentinel organism for monitoring the environmental pollution; a review. Ecological Indicators, 113, 106240.

    Article  CAS  Google Scholar 

  • Bassil, M., Daou, F., Hassan, H., Yamani, O., Kharma, J. A., Attieh, Z., & Elaridi, J. (2018). Lead, cadmium and arsenic in human milk and their socio-demographic and lifestyle determinants in Lebanon. Chemosphere, 191, 911–921.

    Article  CAS  Google Scholar 

  • Berger, B., & Dallinger, R. (1993). Terrestrial snails as quantitative indicators of environmental metal pollution. Environmental Monitoring and Assessment, 25(1), 65–84.

    Article  CAS  Google Scholar 

  • Borjac, J., El Joumaa, M., Kawach, R., Youssef, L., & Blake, D. A. (2019). Heavy metals and organic compounds contamination in leachates collected from Deir Kanoun Ras El Ain dump and its adjacent canal in South Lebanon. Heliyon, 5(8), e02212.

    Article  Google Scholar 

  • Boshoff, M., Jordaens, K., Baguet, S., & Bervoets, L. (2015). Trace metal transfer in a soil–plant–snail microcosm field experiment and biomarker responses in snails. Ecological Indicators, 48, 636–648.

    Article  CAS  Google Scholar 

  • Chen, Y. -G., He, X. -L. -S., Huang, J. -H., Luo, R., Ge, H. -Z., Wołowicz, A., Wawrzkiewicz, M., Gładysz-Płaska, A., Li, B., Yu, Q.-X., Kołodyńska, D., Lv, G. -Y., & Chen, S. -H. (2021). Impacts of heavy metals and medicinal crops on ecological systems, environmental pollution, cultivation, and production processes in China. Ecotoxicology and Environmental Safety, 219, 112336.

    Article  CAS  Google Scholar 

  • Ćirić, J., Cerić, O., Marković, R., Janjić, J., Spirić, D., Popović, M., Pećanac, B., Baltić, B., & Baltić, M. Ž. (2018). Seasonal distributions of heavy metal concentrations in different snail (Helix pomatia) tissues from an urban environment in Serbia. Environmental Science and Pollution Research, 25(33), 33415–33422.

    Article  CAS  Google Scholar 

  • Ćirić, J., Spirić, D., Baltić, T., Lazić, I. B., Trbović, D., Parunović, N., Petronijević, R., & Đorđević, V. (2021). Honey bees and their products as indicators of environmental element deposition. Biological Trace Element Research, 199(6), 2312–2319.

    Article  CAS  Google Scholar 

  • Cravo, A., & Bebianno, M. J. (2005). Bioaccumulation of metals in the soft tissue of Patella aspera: Application of metal/shell weight indices. Estuarine, Coastal and Shelf Science, 65(3), 571–586.

    Article  CAS  Google Scholar 

  • Cravo, A., Bebianno, M. J., & Foster, P. (2004). Partitioning of trace metals between soft tissues and shells of Patella aspera. Environment International, 30(1), 87–98.

    Article  CAS  Google Scholar 

  • Creed, J., Martin, T., & O'Dell, J. (1990). Method 200. 9 determination of trace elements by stabilized temperature graphite furnace atomic absorption spectrometry. Revision 2. 2.

  • Dallinger, R. (1993). Strategies of metal detoxification in terrestrial invertebrates. Ecotoxicology of Metals in Invertebrates, 245.

  • Dar, M. I., Green, I. D., & Khan, F. A. (2019). Trace metal contamination: Transfer and fate in food chains of terrestrial invertebrates. Food Webs, 20, e00116.

    Article  Google Scholar 

  • De Vaufleury, A. (2015). Landsnail for ecotoxicological assessment of chemicals and soil contamination–ecotoxicological assessment of chemicals and contaminated soils using the terrestrial snail, Helix aspersa, at various stage of its life cycle: a review. Environmental indicators, 365–391.

  • De Vaufleury, A. G., & Pihan, F. (2000). Growing snails used as sentinels to evaluate terrestrial environment contamination by trace elements. Chemosphere, 40(3), 275–284.

    Article  Google Scholar 

  • Dobrowolski, R., & Skowrońska, M. (2002). Concentration and discrimination of selected trace metals by freshwater mollusks. Bulletin of Environmental Contamination and Toxicology, 69(4), 509–515.

    Article  CAS  Google Scholar 

  • Dummee, V., Kruatrachue, M., Trinachartvanit, W., Tanhan, P., Pokethitiyook, P., & Damrongphol, P. (2012). Bioaccumulation of heavy metals in water, sediments, aquatic plant and histopathological effects on the golden apple snail in Beung Boraphet reservoir, Thailand. Ecotoxicology and Environmental Safety, 86, 204–212.

    Article  CAS  Google Scholar 

  • European Environmental Agency (EEA). (2006). Priority issues in the Mediterranean environment, Report No 4/2006, ISSN 1725–9177.

  • Eeva, T., Rainio, K., & Suominen, O. (2010). Effects of pollution on land snail abundance, size and diversity as resources for pied flycatcher, Ficedula hypoleuca. Science of the Total Environment, 408(19), 4165–4169.

    Article  CAS  Google Scholar 

  • El-Shenawy, N. S., Mohammadden, A., & Al-Fahmie, Z. H. (2012). Using the enzymatic and non-enzymatic antioxidant defense system of the land snail Eobania vermiculata as biomarkers of terrestrial heavy metal pollution. Ecotoxicology and Environmental Safety, 84, 347–354.

    Article  CAS  Google Scholar 

  • Elaridi, J., Dimassi, H., Al Yamani, O., Estephan, M., & Hassan, H. F. (2021). Determination of lead, cadmium and arsenic in infant formula in the Lebanese market. Food Control, 123, 107750.

    Article  CAS  Google Scholar 

  • Emurotu, J., & Onianwa, P. (2017). Bioaccumulation of heavy metals in soil and selected food crops cultivated in Kogi State, north central Nigeria. Environmental Systems Research, 6(1), 1–9.

    Article  CAS  Google Scholar 

  • EPA, U. (2004). Method 9045D: Soil and Waste pH. Soil and Waste pH, 1–5.

  • EPA, U. (2007). Method 3051A (SW-846): Microwave Assisted Acid Digestion of Sediments, Sludges, and Oils, Revision 1. Washington, DC.

  • Farias, D. R., Hurd, C. L., Eriksen, R. S., & Macleod, C. K. (2018). Macrophytes as bioindicators of heavy metal pollution in estuarine and coastal environments. Marine Pollution Bulletin, 128, 175–184.

    Article  CAS  Google Scholar 

  • Gomot, A., & Pihan, F. (1997). Comparison of the bioaccumulation capacities of copper and zinc in two snail subspecies (Helix). Ecotoxicology and Environmental Safety, 38(2), 85–94.

    Article  CAS  Google Scholar 

  • Harmsen, J. (2007). Measuring bioavailability: From a scientific approach to standard methods. Journal of Environmental Quality, 36(5), 1420–1428.

    Article  CAS  Google Scholar 

  • Ho, Y. (1990). Ulva lactuca as bioindicator of metal contamination in intertidal waters in Hong Kong. Hydrobiologia, 203(1), 73–81.

    Article  CAS  Google Scholar 

  • Itziou, A., & Dimitriadis, V. K. (2011). Introduction of the land snail Eobania vermiculata as a bioindicator organism of terrestrial pollution using a battery of biomarkers. Science of the Total Environment, 409(6), 1181–1192.

    Article  CAS  Google Scholar 

  • Jantataeme, S. I. R. I. W. A. N., Kruatrachue, M., Kaewsawangsap, S., Chitramvong, Y., Sretarugsa, P., & Upatham, E. S. (1996). Acute toxicity and bioaccumulation of lead in the snail, Filopaludina (Siamopaludina) martensi (Frauenfeldt). Journal of the Science Society of Thailand, 22, 237–247.

    Article  CAS  Google Scholar 

  • Kim, H. -T., & Kim, J. -G. (2007). Heavy metal accumulation in Oxyloma hirasei from the Upo wetland. Journal of Ecology and Environment, 30(1), 81–86.

    Article  Google Scholar 

  • Korfali, S. I., & Karaki, H. (2018). Speciation of metals in soils and water: Risk assessment. Environmental Processes, 5(1), 101–125.

    Article  CAS  Google Scholar 

  • Langston, W., & Spence, S. (1995). Biological factors involved in metal concentrations observed in aquatic organisms. Metal Speciation and Bioavailability in Aquatic Systems, 3, 407–478.

    CAS  Google Scholar 

  • Larba, R., & Soltani, N. (2014). Use of the land snail Helix aspersa for monitoring heavy metal soil contamination in Northeast Algeria. Environmental Monitoring and Assessment, 186(8), 4987–4995.

    Article  CAS  Google Scholar 

  • Laskowski, R., & Hopkin, S. P. (1996). Accumulation of Zn, Cu, Pb and Cd in the garden snail (Helix aspersa): Implications for predators. Environmental Pollution, 91(3), 289–297.

    Article  CAS  Google Scholar 

  • Li, C., Sanchez, G. M., Wu, Z., Cheng, J., Zhang, S., Wang, Q., Li, F., Sun, G., & Meentemeyer, R. K. (2020, 2020/05/01/). Spatiotemporal patterns and drivers of soil contamination with heavy metals during an intensive urbanization period (1989–2018) in southern China. Environmental Pollution, 260, 114075.

  • Liang, L., He, B., Jiang, G., Chen, D., & Yao, Z. (2004). Evaluation of mollusks as biomonitors to investigate heavy metal contaminations along the Chinese Bohai Sea. Science of the Total Environment, 324(1–3), 105–113.

    Article  CAS  Google Scholar 

  • Mahmutovic, H., Markovic, R., Janjic, J., Glamoclija, N., Baltic, B., Katanic, N., & Ciric, J. (2018). Concentration of arsenic and heavy metals in snail tissues. Scientific journal Meat Technology, 59(2), 75–79.

  • Massimi, L., Conti, M. E., Mele, G., Ristorini, M., Astolfi, M. L., & Canepari, S. (2019). Lichen transplants as indicators of atmospheric element concentrations: A high spatial resolution comparison with PM10 samples in a polluted area (Central Italy). Ecological Indicators, 101, 759–769.

    Article  CAS  Google Scholar 

  • Mleiki, A., Irizar, A., Zaldibar, B., El Menif, N. T., & Marigómez, I. (2016). Bioaccumulation and tissue distribution of Pb and Cd and growth effects in the green garden snail, Cantareus apertus (Born, 1778), after dietary exposure to the metals alone and in combination. Science of the Total Environment, 547, 148–156.

    Article  CAS  Google Scholar 

  • Mohammadein, A., El-Shenawy, N., & Al-Fahmie, Z. (2013). Bioaccumulation and histopathological changes of the digestive gland of the land snail Eobania vermiculata (Mollusca: Gastropoda), as biomarkers of terrestrial heavy metal pollution in Taif city. Italian Journal of Zoology, 80(3), 345–357.

    Article  CAS  Google Scholar 

  • Nica, D. V., Bordean, D. -M., Borozan, A. B., Gergen, I., Bura, M., & Banatean-Dunea, I. (2013). Use of land snails (Pulmonata) for monitoring copper pollution in terrestrial ecosystems. Reviews of Environmental Contamination and Toxicology, 95–137.

  • Nica, D. V., Bura, M., Gergen, I., Harmanescu, M., & Bordean, D.-M. (2012). Bioaccumulative and conchological assessment of heavy metal transfer in a soil-plant-snail food chain. Chemistry Central Journal, 6(1), 1–15.

    Article  CAS  Google Scholar 

  • Ogunkunle, C. O., & Fatoba, P. O. (2014). Contamination and spatial distribution of heavy metals in topsoil surrounding a mega cement factory. Atmospheric Pollution Research, 5(2), 270–282.

    Article  CAS  Google Scholar 

  • Pauget, B., Gimbert, F., Scheifler, R., Coeurdassier, M., & de Vaufleury, A. (2012). Soil parameters are key factors to predict metal bioavailability to snails based on chemical extractant data. Science of the Total Environment, 431, 413–425.

    Article  CAS  Google Scholar 

  • Peijnenburg, W., & Jager, T. (2003). Monitoring approaches to assess bioaccessibility and bioavailability of metals: Matrix issues. Ecotoxicology and Environmental Safety, 56(1), 63–77.

    Article  CAS  Google Scholar 

  • Proum, S., Santos, J. H., Lim, L. H., & Marshall, D. J. (2016). 2016/11/01/). Metal accumulation in the tissues and shells of Indothais gradata snails inhabiting soft and hard substrata in an acidified tropical estuary (Brunei, South East Asia). Regional Studies in Marine Science, 8, 487–497.

    Article  Google Scholar 

  • Rainbow, P. S. (1995). Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin, 31(4–12), 183–192.

    Article  CAS  Google Scholar 

  • Sánchez-Martín, M., García-Delgado, M., Lorenzo, L., Rodríguez-Cruz, M., & Arienzo, M. (2007). Heavy metals in sewage sludge amended soils determined by sequential extractions as a function of incubation time of soils. Geoderma, 142(3–4), 262–273.

    Article  CAS  Google Scholar 

  • Sawidis, T., Breuste, J., Mitrovic, M., Pavlovic, P., & Tsigaridas, K. (2011, 12//). Trees as bioindicator of heavy metal pollution in three European cities. Environmental Pollution, 159(12), 3560–3570.

  • Scheifler, R., Brahim, M. B., Gomot-de Vaufleury, A., Carnus, J. M., & Badot, P. M. (2003, 4//). A field method using microcosms to evaluate transfer of Cd, Cu, Ni, Pb and Zn from sewage sludge amended forest soils to Helix aspersa snails. Environmental Pollution, 122(3), 343–350.

  • Scheifler, R., De Vaufleury, A., Coeurdassier, M., Crini, N., & Badot, P. M. (2006). Transfer of Cd, Cu, Ni, Pb, and Zn in a soil‐plant‐invertebrate food chain: a microcosm study. Environmental Toxicology and Chemistry: An International Journal, 25(3), 815–822.

  • Sharma, Y. (2009). Histopathology and bioaccumulation of heavy metals (Cu & Pb) in the giant land snail, Archachatina marginata (Swainson). The Open Environmental Pollution & Toxicology Journal, 1(1).

  • Søndergaard, J., Bach, L., & Gustavson, K. (2014, 2014/01/15/). Measuring bioavailable metals using diffusive gradients in thin films (DGT) and transplanted seaweed (Fucus vesiculosus), blue mussels (Mytilus edulis) and sea snails (Littorina saxatilis) suspended from monitoring buoys near a former lead–zinc mine in West Greenland. Marine pollution bulletin, 78(1), 102–109.

  • Stankovic, S., Kalaba, P., & Stankovic, A. R. (2014). Biota as toxic metal indicators. Environmental Chemistry Letters, 12(1), 63–84.

    Article  CAS  Google Scholar 

  • Sturba, L., Fattorini, N., Liberatori, G., Vannuccini, M. L., Nannoni, F., Protano, G., Tursi, A., & Corsi, I. (2020, 2020/10/01/). Multi-model inference analysis of toxicological responses and levels of heavy metals in soft tissue of land snail Cornu aspersum caged in proximity to an industrial setting. Ecological Indicators, 117, 106688.

  • Turekian, K. K., & Wedepohl, K. H. (1961). Distribution of the elements in some major units of the earth’s crust. Geological Society of America Bulletin, 72(2), 175–192.[175:DOTEIS]2.0.CO;2

    Article  CAS  Google Scholar 

  • Udechukwu, B. E., Ismail, A., Zulkifli, S. Z., & Omar, H. (2015). Distribution, mobility, and pollution assessment of Cd, Cu, Ni, Pb, Zn, and Fe in intertidal surface sediments of Sg. Puloh mangrove estuary, Malaysia. Environmental Science and Pollution Research, 22(6), 4242–4255.

  • USEPA. Interim Ecological Soil Screening Level Documents. Retrieved 12 August, 2022. from

  • Vaufleury, A. G., & d., & Pihan, F. (2002). Methods for toxicity assessment of contaminated soil by oral or dermal uptake in land snails: Metal bioavailability and bioaccumulation. Environmental Toxicology and Chemistry: An International Journal, 21(4), 820–827.;2

    Article  Google Scholar 

  • Viard, B., Pihan, F., Promeyrat, S., & Pihan, J. -C. (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 

  • Wazne, M., & Korfali, S. (2016). Spatial and temporal assessment of metal pollution in the sediments of the Qaraoun reservoir. Lebanon. Environmental Science and Pollution Research, 23(8), 7603–7614.

    Article  CAS  Google Scholar 

  • Yap, C., Ismail, A., Tan, S., & Rahim, I. A. (2003). Can the shell of the green-lipped mussel Perna viridis from the west coast of Peninsular Malaysia be a potential biomonitoring material for Cd, Pb and Zn? Estuarine, Coastal and Shelf Science, 57(4), 623–630.

    Article  CAS  Google Scholar 

  • Zhao, Q., Bai, J., Gao, Y., Zhang, G., Lu, Q., & Jia, J. (2021). Heavy metal contamination in soils from freshwater wetlands to salt marshes in the Yellow River Estuary. China. Science of the Total Environment, 774, 145072.

    Article  CAS  Google Scholar 

  • Zrouga, B. A., & K., Mendes, M. P., Falcão, A. P., Almohandes, B. D., Hachicha, M., & Khebour Allouche, F. (2021). Mapping heavy metal (Cu, Zn, and Pb) pollution and ecological risk assessment, in the surroundings of Gabes cement plant—Tunisia. International Journal of Phytoremediation, 23(9), 937–944.

    Article  CAS  Google Scholar 

  • Beeby, A., & Richmond, L. (2011). Sources of variation in the assimilation of lead by a common gastropod sentinel Cantareus aspersus. Science of the Total Environment, 409(24), 5499–5504.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations


Corresponding author

Correspondence to Mahmoud Wazne.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

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 116 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al-Alam, J., Millet, M., Harb, M. et al. Field evaluation of metal bioaccumulation in the gastropod Helix aspersa at agricultural and industrial sites in Lebanon. Environ Monit Assess 195, 197 (2023).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: