Skip to main content

Advertisement

Log in

Short-term influence of phosphate and nitrate on heavy metal accumulation by red alga Acrosorium uncinatum

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

Abstract

Heavy metal accumulation (Cu, Zn, Ni, and Pb) in common marine macroalga, Acrosorium uncinatum under nutrient (phosphate and nitrate) enriched (experiment 1) and starved (experiment 2) conditions over a short exposure period (12 h) were examined in this study. Control was maintained in seawater contained nutrient solution without addition of metals and in seawater alone for experiment 1 and 2, respectively. Among the four metals studied, the accumulation of Zn, Ni, and Pb was considerably lower than Cu. The accumulation factor for all metals varies greatly in different nutrient concentrations, but it increases as the exposure of metal concentration decreases in both the experiments. The results of the present findings established that this macroalga is an accumulator of metals Cu, Zn, Ni, and Pb and have the potential to accumulate these metals even in a short time exposure period (12 h). Even though metal accumulation by A. uncinatum largely depends on the available concentration in the medium, nutrients like phosphate and nitrate can affect the accumulation significantly.

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.

Similar content being viewed by others

References

  • Andrade, L. R., Farina, M., & Filho, A. G. M. (2002). Role of Padina gymnospora (Dictyotales, Phaeophyceae) cell walls in cadmium accumulation. Phycologia, 41, 39–48.

    Google Scholar 

  • Angelone, M., & Bini, C. (1992). Trace elements concentrations in soils and plants of Western Europe. In D. C. Adriano (Ed.), Biogeochemistry of trace metals (pp. 19–60). Boca Raton: Lewis.

    Google Scholar 

  • Ariza, M. E., Bijur, G. N., & Williams, M. V. (1999). Environmental metal pollutants, reactive oxygen intermediaries and genotoxicity. Boston: Kluwer.

    Google Scholar 

  • Barraza, J. E., & Carballeira, A. (1999). Chlorophyll fluorescence analysis and cadmium–copper bioaccumulation in Ulva rigida (C. Agardh). Boletín del Instituto Español de Oceanografía, 15, 395–399.

    Google Scholar 

  • Bryan, G. W. (1983). Brown seaweed, Fucus vesiculosus, and the gastropod Littorina littoralis, as indicators of trace metal availability in estuaries. The Science of the Total Environment, 28, 91–104. doi:10.1016/S0048-9697(83)80010-2.

    Article  CAS  Google Scholar 

  • Burdin, K. S., & Bird, K. T. (1994). Heavy metal accumulation by car-rageenan and agar producing algae. Botanica Marina, 37, 467–470.

    Article  CAS  Google Scholar 

  • Carreras, H. A., & Pignata, M. L. (2007). Effects of the heavy metals Cu(2+), Ni(2+), Pb(2+), and Zn(2+) on some physiological parameters of the lichen Usnea amblyoclada. Ecotoxicology and Environmental Safety, 67, 59–66. doi:10.1016/j.ecoenv.2006.05.005.

    Article  CAS  Google Scholar 

  • Chan, S. M., Wang, W., & Ni, I. (2003). The uptake of Cd, Cr, and Zn by the macroalga Enteromorpha crinita and subsequent transfer to the marine herbivorous rabbitfish, Sigunus canaliculatus. Archives of Environmental Contamination and Toxicology, 44, 298–306. doi:10.1007/s00244-002-2077-3.

    Article  CAS  Google Scholar 

  • Craigie, J. S. (1990). Cell walls. In K. M. Cole, & R. G. Sheath (Eds.), Biology of the red algae (pp. 221–257). New York: Cambridge University Press.

    Google Scholar 

  • Esen, N., Topcuoglu, S., Egilli, E., & Kut, D. (1999). Comparison of trace metal concentrations in sediments and algae samples from the Kucukcekmece Lagoon and Marmara Sea. Journal of Radioanalytical and Nuclear Chemistry, 240, 673–676. doi:10.1007/BF02349432.

    Article  CAS  Google Scholar 

  • Farina, J. M., Castilla, J. C., & Ojeda, F. B. (2003). The “idiosyncratic” effect of a “sentinel” species on contaminated rocky intertidal communities. Ecological Society of America, 13, 1533–1552.

    Google Scholar 

  • Ferletta, M., Bramer, P., Semesi, A. K., & Bjork, M. (1996). Heavy metal contents in macroalgae in the Zanzibar channel—An initial study. In M. Bjork, A. K. Semesi, M. Perdersen, & B. Bergman (Eds.), Current trends in marine botanical research in the East African Region. Proceedings on the Biology of Macroalgae and Seagrasses in the Western Indian Ocean Stockholm, Sida.

  • Filho, G. M. A., Andrade, L. R., Karez, C. S., Farina, M., & Pfeiffer, W. C. (1999). Brown algae species as biomonitors of Zn and Cd at Sepetiba Bay, Rio de Janeiro, Brazil. Marine Environmental Research, 48, 213–224. doi:10.1016/S0141-1136(99)00042-2.

    Article  Google Scholar 

  • Fisher, W. S. (1986). Structure and functions of oyster hemocytes. In Brehelin (Ed.), Immunity in invertebrates (pp. 25–35). Heidelberg: Springer.

    Google Scholar 

  • Fisher, N. S., & Fabris, J. G. (1982). Complexation of Cu, Zn, and Cd by metabolites excreted from marine diatoms. Marine Chemistry, 11, 245–255. doi:10.1016/0304-4203(82)90019-6.

    Article  CAS  Google Scholar 

  • Fisher, N. S., Bore, M., & Teyssie, J. (1984). Accumulation and toxicity of cadmium, zinc, silver and mercury in four marine phytoplankters. Marine Ecology Progress Series, 18, 201–214. doi:10.3354/meps018201.

    Article  CAS  Google Scholar 

  • Fityanos, K., Evgenidou, E., & Zachariadis, G. (1999). Use of macroalgae as biological indicators of heavy metal pollution in Thermaikos Gulf, Greece. Bulletin of Environmental Contamination and Toxicology, 62, 630–637. doi:10.1007/s001289900921.

    Article  Google Scholar 

  • Galloway, J. N., Thornton, J. D., Norton, S. A., Volcho, H. L., & McLean, R. A. (1982). Trace metals in atmospheric deposition: A review and assessment. Atmospheric Environment, 16, 1677. doi:10.1016/0004-6981(82)90262-1.

    Article  CAS  Google Scholar 

  • Gothberg, A., Greger, M., Holm, K., & Bengtsson, B. E. (2004). Influence of nutrient levels on uptake and effects of mercury, cadmium, and lead in water spinach. Journal of Environmental Quality, 33, 1247–1255.

    Google Scholar 

  • Guven, K. C., Sayg, N., & Ozturk, B. (1993). Surveys of metal contents of Bosphorus algae, Zostera marina. Botanica Marina, 36, 175–178.

    Article  CAS  Google Scholar 

  • Guven, K. C., Okus, E., Topcuoglu, S., Esen, N., Kucukcezzar, R., Seddigh, E., et al. (1998). Heavy metal accumulation in algae and sediments of the Black Sea coast of Turkey. Toxicological and Environmental Chemistry, 67, 435–440. doi:10.1080/02772249809358633.

    Article  CAS  Google Scholar 

  • Guven, K. C., Topcuoglu, S., Kut, D., Esen, N., Erenturk, N., Sayg, N., et al. (1992). Metal uptake by Black Sea algae. Botanica Marina, 35, 337–340.

    Article  CAS  Google Scholar 

  • Haglund, K., Bjorklund, M., Gunnare, S., Sandberg, A., Olander, U., & Pedersen, M. (1996). New method for toxicity assessment in marine and brackish environments using the macroalga Gracilaria tenuistipitata (Gracilariales, Rhodophyta). Hydrobiologia, 326/327, 317–325. doi:10.1007/BF00047825.

    Article  CAS  Google Scholar 

  • Hall, J., Healey, F. P., & Robinson, G. G. C. (1989). The interaction of chronic copper toxicity with nutrient limitation in chemostat cultures of Chlorella. Aquatic Toxicology (Amsterdam, Netherlands), 14, 15–26. doi:10.1016/0166-445X(89)90052-0.

    CAS  Google Scholar 

  • Hardisson, A., Frias, I., Bonis, A., De Lozano, G., & Baez, A. (1998). Mercury in algae of the Canary Islands littoral. Environment International, 24, 945–950. doi:10.1016/S0160-4120(98)00081-6.

    Article  CAS  Google Scholar 

  • Ho, Y. B. (1990). Metals in Ulva lactuca. Bulletin of Marine Science, 47, 79–85.

    Google Scholar 

  • Imber, B. E., Robinson, M. G., Ortega, A. M., & Burton, J. D. (1985). Complexation of zinc by exudates from Skeletoma costatum grown in culture. Marine Chemistry, 16, 131–139. doi:10.1016/0304-4203(85)90018-0.

    Article  CAS  Google Scholar 

  • Kaewsarn, P., & Yu, Q. (2001). Cadmium removal from aqueous solutions by pre-treated biomass of marine alga Padina sp. Environmental Pollution, 112, 209–213. doi:10.1016/S0269-7491(00)00114-7.

    Article  CAS  Google Scholar 

  • Kelly, M. (1998). Mining and the freshwater environment. London: Elsevier Applied Science.

    Google Scholar 

  • Kupper, F. C., Schweigert, N., Ar Gall, E., Legendre, J. M., Vilter, H., & Kloareg, B. (1998). Iodine uptake in laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta, 207, 163–171. doi:10.1007/s004250050469.

    Article  Google Scholar 

  • Kut, D., Topcuoglu, S., Esen, N., Kucukcezzar, R., & Guven, K. C. (2000). Trace metals in marine algae samples from the Bosphorus. Water, Air, and Soil Pollution, 118, 27–33. doi:10.1023/A:1005149500870.

    Article  CAS  Google Scholar 

  • Kuyucak, N., & Volesky, B. (1989). Accumulation of cobalt by marine alga and sediment samples. Biotechnology and Bioengineering, 33, 809–814. doi:10.1002/bit.260330703.

    Article  CAS  Google Scholar 

  • Lee, W., & Wang, W. (2001). Metal accumulation in the green macroalga Ulva fasciata: Effects of nitrate, ammonium and phosphate. The Science of the Total Environment, 278, 11–22. doi:10.1016/S0048-9697(00)00884-6.

    Article  CAS  Google Scholar 

  • Leland, H. V., Copenhauer, E. D., & Corril, L. S. (1974). Heavy metals and other trace elements. Journal of Water Pollution Control, 46, 1452–1476.

    CAS  Google Scholar 

  • Leland, H. V., Luoma, S. N., & Fielden, J. M. (1979). Bioaccumulation and toxicity of heavy metals and deleted trace elements. Journal of Water Pollution Control, 56, 1592–1616.

    Google Scholar 

  • Levine, H. G. (1984). The use of seaweeds for monitoring coastal waters. In L. E. Shubert (Ed.), Algae as ecological indicators (pp. 189–210). London: Academic.

    Google Scholar 

  • Macfie, S. M., & Welbourn, P. M. (2000). The cell wall as a barrier to uptake of metal ions in the unicellular green alga Chlamydomonas reinhardtii (Chlorophyceae). Archives of Environmental Contamination and Toxicology, 39, 413–419. doi:10.1007/s002440010122.

    Article  CAS  Google Scholar 

  • Mamboya, F. A. (2007). Heavy metal contamination and toxicity: Studies of macroalgae from the Tanzanian Coast. Doctoral thesis submitted to Department of Botany, Stockholm University.

  • Markham, J. W., Kremer, B. P., & Sperling, K. R. (1980). Cadmium effects on growth and physiology of Ulva lactuca. Helgolaender Meeresuntersuchungen, 33, 103–110. doi:10.1007/BF02414739.

    Article  Google Scholar 

  • Muse, J. O., Stripeikis, J. D., Fernàndez, F. M., d’Huicque, L., Tudino, M. B., Carducci, C. N., et al. (1999). Seaweeds in the assessment of heavy metal pollution in the Gulf San Jorge, Argentina. Environmental Pollution, 104, 315–322. doi:10.1016/S0269-7491(98)00096-7.

    Article  CAS  Google Scholar 

  • Peng, H., Yang, X., & Tian, S. (2005). Accumulation and ultrastructural distribution of copper in Elsholtzia splendens. Journal of Zhejiang University. Science, 6, 311–318. doi:10.1631/jzus.2005.B0311.

    Article  CAS  Google Scholar 

  • Phillips, D. J. H. (1997). The use of biological indicator organisms to monitor trace metal pollution in marine and estuarine environment—A review. Environmental Pollution, 13, 281–317.

    Google Scholar 

  • Rai, L. C., Gaur, J. P., & Kumar, H. D. (1981). Phycology and heavy-metal pollution. Biological Reviews of the Cambridge Philosophical Society, 56, 99–151. doi:10.1111/j.1469-185X.1981.tb00345.x.

    Article  CAS  Google Scholar 

  • Rice, D. L., & Lapointe, B. F. (1981). Experimental outdoor studies with Ulva fasciata Delile. II. Trace metal chemistry. Journal of Experimental Marine Biology and Ecology, 54, 1–11. doi:10.1016/0022-0981(81)90098-8.

    Article  CAS  Google Scholar 

  • Salgado, L. T., Andrade, L. R., & Amado, G. M. F. (2005). Localization of specific monosaccharides in cells of the brown alga Padina gymnospora and the relation to heavy-metal accumulation. Protoplasma, 225, 123–128. doi:10.1007/s00709-004-0066-2.

    Article  CAS  Google Scholar 

  • Sawidis, T., & Voulgaropoulos, N. (1986). Seasonal bioaccumulation of iron, cobalt, copper in marine algae from Thermaikos Gulf of the Northem Aegean Sea, Greece. Marine Environmental Research, 19, 39–47. doi:10.1016/0141-1136(86)90038-3.

    Article  CAS  Google Scholar 

  • Sawidis, T., Brown, M. T., Zachariadis, G., & Sratis, I. (2001). Trace metal concentrations in marine macroalgae from different biotopes in the Aegean Sea. Environment International, 27, 43–47. doi:10.1016/S0160-4120(01)00052-6.

    Article  CAS  Google Scholar 

  • Seeliger, U., & Edwards, P. (1979). Fate of biologically accumulated copper in growing and decomposing thalli of two benthic red marine algae. Journal of the Marine Biological Association of the United Kingdom, 59, 227–238.

    Article  CAS  Google Scholar 

  • Sharma, R. M., & Azeez, P. A. (1998). Accumulation of copper and cobalt by blue-green algae at different temperatures. International Journal of Environmental Analytical Chemistry, 32, 87–95. doi:10.1080/03067318808078419.

    Article  Google Scholar 

  • Silverberg, B. A. (1975). Ultrastructural localization of lead in Stigeoclonium tenue (Chlorophyceae, Ulotrichales) as demonstrated by cytochemical and X-ray microanalysis. Phycologia, 14, 265–274.

    CAS  Google Scholar 

  • Skaar, H., Rystad, B., & Jensen, A. (1974). The uptake of 63Ni by the diatom Phaeodactylum tricornutum. Physiologia Plantarum, 32, 353–358. doi:10.1111/j.1399-3054.1974.tb03150.x.

    Article  CAS  Google Scholar 

  • Stengel, D. B., Macken, A., Morrison, L., & Morley, N. (2004). Zinc concentrations in marine macroalgae and a lichen from western Ireland in relation to phylogenetic grouping, habitat and morphology. Marine Pollution Bulletin, 48, 902–909. doi:10.1016/j.marpolbul.2003.11.014.

    Article  CAS  Google Scholar 

  • Stromgren, T. (1980). The effect of dissolved copper on the increase in length of four species of intertidal fucoid algae. Marine Environmental Research, 3, 5–13. doi:10.1016/0141-1136(80)90032-X.

    Article  CAS  Google Scholar 

  • Subramanian, V. V., Sivasubramanian, V., & Gowrinathan, K. P. (1994). Uptake and recovery of heavy metals by immobilized cells of aphanocapsa pulchara (Kutz.) rabenth. Journal of Environmental Science and Health, 29, 723–733. doi:10.1080/10934529409376142.

    Article  Google Scholar 

  • Topcuoglu, S., Guven, K. C., Balkis, N., & Kirbasoglu, C. (2003). Heavy metal monitoring of marine algae from the Turkish Coast of the Black Sea. Chemosphere, 52, 1683–1688. doi:10.1016/S0045-6535(03)00301-1.

    Article  CAS  Google Scholar 

  • Wang, W. X., & Dei, R. C. H. (2001a). Metal uptake in a coastal diatom influenced by major nutrients (N, P, Si). Water Research, 35, 315–321. doi:10.1016/S0043-1354(00)00256-6.

    Article  CAS  Google Scholar 

  • Wang, W. X., & Dei, R. C. H. (2001b). Effect of major nutrient additions on metal uptake in marine phytoplankton. Environmental Pollution, 111, 233–240. doi:10.1016/S0269-7491(00)00071-3.

    Article  CAS  Google Scholar 

  • Wang, W. X., & Dei, R. C. H. (2001c). Influence of phosphate and silicate on Cr VI and Se IV uptake in marine phytoplankton. Aquatic Toxicology (Amsterdam, Netherlands), 52, 39–47. doi:10.1016/S0166-445X(00)00132-6.

    CAS  Google Scholar 

  • Wang, W. X., & Fisher, N. S. (1998). Accumulation of trace elements in a marine copepod. Limnology and Oceanography, 43, 273–283.

    Article  CAS  Google Scholar 

  • Wang, M., Wang, D., Wang, G., Huang, X., & Hong, H. (2007). Influence of N, P additions on the transfer of nickel from phytoplankton to copepods. Environmental Pollution, 148, 679–687. doi:10.1016/j.envpol.2006.11.014.

    Article  CAS  Google Scholar 

  • Webster, E. A., & Gadd, G. M. (1996). Perturbation of monovalent cation composition in Ulva lactuca by cadmiun, copper and zinc. Biometals, 9, 51–56.

    CAS  Google Scholar 

  • Wekwe, W. W., Othman, O. C., & Khan, M. R. (1989). Seaweeds as heavy metal pollution indicators. In M. R. Khan, & H. J. Gijzan (Eds.), Environmental pollution and its management in Eastern Africa (pp. 241–248). Dares Salaam: University of Dares Salaam.

    Google Scholar 

  • Zhou, X. L., & Wangersky, P. J. (1985). Copper complexing capacity in cultures of Phaeodactylum tricornutum. Marine Chemistry, 17, 301–312. doi:10.1016/0304-4203(85)90003-9.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to S. Sivakumar or Y. C. Song.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sivakumar, S., Song, Y.C., Park, I.S. et al. Short-term influence of phosphate and nitrate on heavy metal accumulation by red alga Acrosorium uncinatum . Environ Monit Assess 165, 449–460 (2010). https://doi.org/10.1007/s10661-009-0958-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-009-0958-x

Keywords

Navigation