Skip to main content
Log in

Trace and rare earth elements in phytoplankton from the Tyrrhenian Sea (Italy)

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

Abstract

Plankton plays a very crucial role in bioaccumulation and transfer of metals in the marine food web and represents a suitable bioindicator of the occurrence of trace and rare earth elements in the ecosystem. Trace elements and REEs were analyzed by ICP-MS in phytoplankton samples from the northwestern Mediterranean Sea. Metal concentrations in phytoplankton were found strongly influenced by seasons and depth of collection (− 30 m, − 50 m). Principal component analysis (PCA) has shown that Al, As, Cr, Cu, Ga, and Sn concentrations were related to summer and autumn in samples collected at 30 m depth, while Fe, Mn, Ni, V, and Zn levels related strongly with summer and spring at 50 m depth. Fe, Al, and Zn were the most represented elements in all samples (mean values respectively in the ranges 4.2–8.2, 9.6–13, and 1.0–4.4 mg kg−1) according to their widespread presence in the environment and in the earth crust. Principal component analysis (PCA) performed on REEs showed that mostly all lanthanides’ concentrations strongly correlate with summer and autumn seasons (− 30 m depth); the highest ∑REE concentration (75 µg kg−1) was found in winter. Phytoplankton REE normalized profile was comparable to those of other marine biota collected in the same area according to the suitability of lanthanides as geological tracers.

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The datasets used and analyzed during the current study are available from the corresponding author on request.

References

  • Albarico, F. P. J. B., Lim, Y. C., Chen, C.-W., Chen, C. H., Wang, M.-H., & Dong, C.-D. (2024). Linking seasonal plankton succession and cellular trace metal dynamics in marine assemblages. Science of the Total Environment, 907, 167805.

    Article  CAS  Google Scholar 

  • Ambrose, P. (1999). Cetacean sanctuary in the Mediterranean Sea. Marine Pollution Bulletin, 38(9), 748.

    Google Scholar 

  • Anastopoulos, I., Bhatnagar, A., & Lima, E. C. (2016). Adsorption of rare earth metals: A review of recent literature. Journal of Molecular Liquids, 221, 954–962.

    Article  CAS  Google Scholar 

  • Annabi-Trabelsi, N., Guermazi, W., Karam, Q., Ali, M., Uddin, S., Leignel, V., & Ayadi, H. (2021). Concentrations of trace metals in phytoplankton and zooplankton in the Gulf of Gabès Tunisia. Mar Pollut Bull., 168, 112392.

    Article  CAS  Google Scholar 

  • Battuello, M., Brizio, P., Sartor, R. M., Nurra, N., Pessani, D., Abete, M. C., & Squadrone, S. (2016). Zooplankton from a Northwestern Mediterranean area as a model of metal transfer in a marine environment. Ecological Indicators, 66, 440–451.

    Article  CAS  Google Scholar 

  • Bau, M., & Dulski, P. (1996). Anthropogenic origin of positive gadolinium anomalies in river waters. Earth and Planetary Science Letters, 143, 245–255.

    Article  CAS  Google Scholar 

  • Bau, M., Knappe, A., & Dulski, P. (2006). Anthropogenic gadolinium as a micropollutant in river waters in Pennsylvania and in Lake Erie, northeastern United States. Geochemistry, 66(2), 143–152. https://doi.org/10.1016/j.chemer.2006.01.002

  • Browning, T. J., Achterberg, E. P., Engel, A., et al. (2021). Manganese co-limitation of phytoplankton growth and major nutrient drawdown in the Southern Ocean. Nat Communications, 12, 884.

    Article  CAS  Google Scholar 

  • Byrne, R. H., & Kim, K. H. (1990). Rare earth element scavenging in seawater. Geochimica Et Cosmochimica Acta, 54(10), 2645–2656.

    Article  CAS  Google Scholar 

  • Chiocci, F. L., La Monica, G. B. (1996). Analisi sismostratigrafica della piattaforma conti-nentale. In: Il Mare del Lazio – Elementi di oceanografia fisica e chimica, biologiae geologia marina, clima meteomarino, dinamica dei sedimenti ed apporti con-tinentale. Regione Lazio, Tip. Borgia, Roma, pp. 40–61.

  • Da Silva, J. F., Williams, R. J. P. (2001). The biological chemistry of the elements: The inorganic chemistry of life. Oxford University Press.

  • Dang, D. H., Wang, W., Winkler, G., & Chatzis, A. (2023). Rare earth element uptake mechanisms in plankton in the Estuary and Gulf of St. Lawrence, Science of the Total Environment, 860, 160394.

    Article  CAS  Google Scholar 

  • Duce, A., Liss, P. S., Merrill, J. T., Atlas, E. L., Buat-Menard, P., Hicks, B. B., Miller, J. M., Prospero, J. M., Arimoto, R., Church, T. M., EllisW, G. J. N., Hansen, L., Jickells, T. D., Knap, A. H., Reinhardt, K. H., Schneider, B., Soudine, A., Tokos, J. J., Tsunogai, S., … Zhou, M. (1991). The atmospheric input of trace species to the world oceans. Global Biogeochem Cycl., 5, 193–259.

    Article  CAS  Google Scholar 

  • Echeveste, P., Agustí, S., & Tovar-Sánchez, A. (2012). Toxic thresholds of cadmium and lead to oceanic phytoplankton: Cell size and ocean basin-dependent effects. Environ Toxicol Chem. 31(8), 1887–94. Gasparini G.P., Zodiatis G., Astraldi M., Galli C., Sparnocchia S. 1999, Winter Intermediate water 575 lenses in the Ligurian Sea. Journal of Marine Systems, 20, 319–332.

    Google Scholar 

  • Golding, L. A., Angel, B. M., Batley, G. E., Apte, S. C., Krassoi, R., & Doyle, C. J. (2015). Derivation of a water quality guideline for aluminium in marine waters. Environmental Toxicology and Chemistry, 34, 141–151.

    Article  CAS  Google Scholar 

  • Hara, Y., Obata, H., Doi, T., Hongo, Y., Gamo, T., Takeda, S., & Tsuda, A. (2009). Rare earth elements in seawater during an iron-induced phytoplankton bloom of the western subarctic Pacific (SEEDSII). Deep Sea Research Part II: Topical Studies in Oceanography, 56(26), 2839–2851.

    Article  CAS  Google Scholar 

  • Kellogg, R. M., Moosburner, M. A., Cohen, N. R., et al. (2022). Adaptive responses of marine diatoms to zinc scarcity and ecological implications. Nat Communications, 13, 1995.

    Article  CAS  Google Scholar 

  • La Fontaine, S., Quinn, J. M., Nakamoto, S. S., Page, M. D., Göhre, V., Moseley, J. L., & Merchant, S. (2002). Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryotic cell, 1(5), 736–757.

    Article  Google Scholar 

  • Le Goff, S., Barrat, J., Chauvaud, L., Paulet, Y., Gueguen, B., & Salem, D. B. (2019). Compound specific recording of gadolinium pollution in coastal waters by great scallop. Scientific Reports, 9, 8015.

    Article  Google Scholar 

  • Leardi, R., Melzi, C., Polotti, G. (2014). CAT (Chemometric Agile Tool), freely downloadable fromhttp://gruppochemiometria.it/index.php/software Accessed Mar 2023 Principal component analysis. Analytical Methods 6:2812–2831.

  • Maldonado, M. T., Allen, A. E., Chong, J. S., Lin, K., Leus, D., Karpenko, N., & Harris, S. L. (2006). Copper-dependent iron transport in coastal and oceanic diatoms. Limnology and Oceanography, 51(4), 1729–1743.

    Article  CAS  Google Scholar 

  • Martino, C., et al. (2018). Gadolinium perturbs expression of skeletogenic genes, calcium uptake and larval development in phylogenetically distant sea urchin species. Aquatic Toxicology, 194, 57–66.

    Article  CAS  Google Scholar 

  • Mason, R. P. (2013). Trace metals in aquatic systems. John Wiley & Sons. Masuda, A., 1975. Abundance of monoisotopic REE, consistent with Leedey chondrite values. Geochemical Journal, 9, 183–184.

    Google Scholar 

  • Merschel, G., & Bau, M. (2015). Rare earth elements in the aragonitic shell of freshwater mussel Corbicula fuminea and the bioavailability of anthropogenic lanthanum, samarium and gadolinium in river water. Science of the Total Environment, 533, 91–101.

    Article  CAS  Google Scholar 

  • Moore, R. M., Webb, R., Tokarczyk, R., & Wever, R. (1996). Bromoperoxidase and iodoperoxidase enzymes and production of halogenated methanes in marine diatom cultures. Journal of Geophysical Research, 101, 20899–20908.

    Article  CAS  Google Scholar 

  • Moore, J. K., Doney, S. C., Lindsay, K. (2004). Upper ocean ecosystem dynamics and iron cycling in a global three‐dimensional model. Global Biogeochemical Cycles, 18(4).

  • Neira, P., Romero-Freire, A., Basallote, M. D., Qiu, H., Cobelo-Garcıa, A., & Canovas, C. R. (2022). Review of the concentration, bioaccumulation, and effects of lanthanides in marine systems. Frontiers in Marine Science, 9, 920405.

    Article  Google Scholar 

  • Ostrakhovitch, H.A., Chapter 33 - Tin, Editor(s): Gunnar F. Nordberg, Max Costa, Handbook on the toxicology of metals (fifth edition), Academic Press, 2022, 807–856.

  • Paimpillil, J. S., Thresiamma, J., Rejomon, G., Gerson, V. J. (2010). Metals in coastal zooplanktons – A coastal living resource hazard. Indian Geological Congres, 199–207

  • Papry, R. I., Omori, Y., Fujisawa, S., Al Mamun, M. A., Miah, S., Mashio, A. S., Maki, T., & Hasegawa, H. (2020). Arsenic biotransformation potential of marine phytoplankton under a salinity gradient. Algal Research, 47(2020), 101842.

    Article  Google Scholar 

  • Quigg, A., Finkel, Z. V., Irwin, A. J., Rosenthal, Y., Ho, T. Y., Reinfelder, J. R., & Falkowski, P. G. (2003). The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature, 425(6955), 291–294.

    Article  CAS  Google Scholar 

  • Ragsdale, S. W. (1998). Nickel biochemistry. Current Opinion in Chemical Biology, 2(2), 208–215.

    Article  CAS  Google Scholar 

  • Rahman, M. A., Hasegawa, H., & Lim, R. P. (2012). Bioaccumulation, biotransformation, and trophic transfer of arsenic in the aquatic food chain. Environmental Research, 116, 118–135.

    Article  Google Scholar 

  • Renzi, M., Perra, G., Lobianco, A., Mari, E., Guerranti, C., Specchiulli, A., Pepi, M., & Focardi, S. (2009). Environmental quality assessment of the marine reserve of the Tuscan Archipelago, Central Tyrrhenian Sea (Italy). Chemical Ecology, 26, 299–317.

    Article  Google Scholar 

  • Roveta, C., Annibaldi, A., Afghan, A., Calcinai, B., Di Camillo, C. G., Gregorin, C., Illuminati, S., Pulido Mantas, T., Truzzi, C., & Puce, S. (2021). Biomonitoring of heavy metals: The unexplored role of marine sessile taxa. Applied Sciences, 11, 580.

    Article  CAS  Google Scholar 

  • Salgado-Hernanz, P. M., Racault, M. F., Font-Muñoz, J. S., & Basterretxea, G. (2019). Trends in phytoplankton phenology in the Mediterranean Sea based on ocean-colour remote sensing. Remote Sensing of Environment, 221, 50–64.

    Article  Google Scholar 

  • Schier, K., Ernst, D. M., Cordeiro, M., de Sousa, I., Garbe-Schönberg, D., Kuhn, T., Hein, J. R., & Bau, M. (2021). Gallium-aluminum systematics of marine hydrogenetic ferromanganese crusts: Inter-oceanic differences and fractionation during scavenging. Geochimica Et Cosmochimica Acta, 310, 187–204.

    Article  CAS  Google Scholar 

  • Schiffer, S., & Liber, K. (2017). Toxicity of aqueous vanadium to zooplankton and phytoplankton species of relevance to the Athabasca oil sand region. Ecotoxicology and Environmental Safety, 137, 1–11.

    Article  CAS  Google Scholar 

  • Semeniuk, D. M., Maldonado, M. T., & Jaccard, S. L. (2016). Chromium uptake and adsorption in marine phytoplankton – Implications for the marine chromium cycle. Geochimica Et Cosmochimica Acta, 184, 41–54.

    Article  CAS  Google Scholar 

  • Sun, T., Wu, H., Wang, X., Ji, C., Shan, X., & Li, F. (2020). Evaluation on the biomagnification or biodilution of trace metals in global marine food webs by meta-analysis. Environmental pollution, 264, 113856. https://doi.org/10.1016/j.envpol.2019.113856

  • Squadrone, S., Brizio, P., Stella, C., Prearo, M., Pastorino, P., Serracca, L., Ercolini, C., & Abete, M. C. (2016). Presence of trace metals in aquaculture marine ecosystems of the northwestern Mediterranean Sea (Italy). Environmental Pollution, 215, 77–83.

    Article  CAS  Google Scholar 

  • Squadrone, S., Brizio, P., Battuello, M., Nurra, N., Mussat Sartor, R., Benedetto, A., Pessani, D., & Abete, M. C. (2017). A first report of rare earth elements in northwestern Mediterranean seaweeds. Marine Pollution Bulletin, 122(1–2), 236–242.

    Article  CAS  Google Scholar 

  • Squadrone, S., Brizio, P., Stella, C., Mantia, M., Battuello, M., Nurra, N., Mussat Sartor, R., Orusa, R., Robetto, S., Brusa, F., Mogliotti, P., Garrone, A., & Abete, M. C. (2019). Rare earth elements in marine and terrestrial matrices of Northwestern Italy: Implications for food safety and human health. Science of the Total Environment, 660, 1383–1391.

    Article  CAS  Google Scholar 

  • Strady, E., Kim, I., Radakovitch, O., & Kim, G. (2015). Rare earth element distributions and fractionation in plankton from the northwestern Mediterranean Sea. Chemosphere, 119, 72–82.

    Article  CAS  Google Scholar 

  • Sutak, R., Camadro, J. M., Lesuisse, E. (2020). Iron Uptake Mechanisms in Marine Phytoplankton. Front Microbiol. 11:566691. Tagliabue, A., Bopp, L., Aumont, O., Arrigo, K. R. 2009. Influence of light and temperature on the marine iron cycle: From theoretical to global modeling. Global Biogeochemical Cycles, 23(2).

  • Tsvetkov, P., Coy, S., Petrova, B., Dreishpoon, M., Verma, A., Abdusamad, M., et al. (2022). Copper induces cell death by targeting lipoylated TCA cycle proteins. Science, 375, 1254–1261.

    Article  CAS  Google Scholar 

  • Twining, B. S., & Baines, S. B. (2013). The trace metal composition of marine phytoplankton. Annual Review of Marine Science, 5, 191–215.

    Article  Google Scholar 

  • Uddin, S., Bebhehani, M., Sajid, S., & Karam, Q. (2019). Concentration of 210Po and 210Pb in macroalgae from the northern Gulf. Marine Pollution Bulletin, 145, 474–479.

    Article  CAS  Google Scholar 

  • Uthus, E. O. (2003). Arsenic essentiality: A role affecting methionine metabolism. Journal of Trace Elements in Experimental Medicine, 16(4), 345–355.

    Article  CAS  Google Scholar 

  • Wang, W. X., Dei, R. C., & Hong, H. (2005). Seasonal study on the Cd, Se, and Zn uptake by natural coastal phytoplankton assemblages. Environmental Toxicology and Chemistry, 24(1), 161–169.

    Article  Google Scholar 

  • Xu, Y., & Morel, F. M. (2013). Cadmium in marine phytoplankton. Metal Ions in Life Sciences, 11, 509–528.

    Article  CAS  Google Scholar 

  • Ye, N., Han, W., Toseland, A., et al. (2022). The role of zinc in the adaptive evolution of polar phytoplankton. Nature Ecology & Evolution, 6, 965–978.

    Article  Google Scholar 

  • Zhang, L. (2022). Copper uptake and subcellular distribution in five marine phytoplankton species. Frontiers in Marine Science, 9, 1084266.

    Article  Google Scholar 

  • Zhou, L., Tan, Y., Huang, L., et al. (2018). Aluminum effects on marine phytoplankton: Implications for a revised iron hypothesis (iron–aluminum hypothesis). Biogeochemistry, 139(2), 123.

    Article  CAS  Google Scholar 

  • Zocher, A. L., Klimpel, F., Kraemer, D., & Bau, M. (2022). Naturally grown duckweeds as quasi-hyperaccumulators of rare earth elements and yttrium in aquatic systems and the biounavailability of gadolinium-based MRI contrast agents. Science of The Total Environment, 838, 155909. https://doi.org/10.1016/j.scitotenv.2022.155909

Download references

Acknowledgements

Authors greatly appreciate the contribution of the anonymous reviewers to improve the manuscript.

Funding

This research was funded by the Italian Health Ministry Research Grants (Project n. IZS PLV 20/16 RC).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Sampling planning and sample collections were the responsibility of NN, RMS, and MB. Examination and data collection were performed by AG, RA, and E del B. Methodology optimization and chemical analysis were performed by AG and GB. Statistical evaluation was the responsibility of AT and SS. The first draft of the manuscript was written by E del B, LF, NN, and SS. All authors discussed the results and contributed to the final manuscript. Review and editing of the final manuscript was performed by SS and MCA. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Stefania Squadrone.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethical approval

All authors have read, understood, and have complied as applicable with the statement on “Ethical responsibilities of Authors” as found in the Instructions for Authors.

Consent to participate

The authors consent to participate in the research and elaboration of the manuscript.

Consent for publication

The authors consent to publish this manuscript.

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 (DOC 235 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

del Buono, E., Nurra, N., Sartor, R.M. et al. Trace and rare earth elements in phytoplankton from the Tyrrhenian Sea (Italy). Environ Monit Assess 196, 399 (2024). https://doi.org/10.1007/s10661-024-12552-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-024-12552-y

Keywords

Navigation