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The Korean Society of Phycology (한국조류학회(藻類))
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Bioaccumulation of copper and zinc by the giant kelp Macrocystis pyrifera

  • Evans, La Kenya (Department of Biology, San Diego State University) ;
  • Edwards, Matthew S. (Department of Biology, San Diego State University)
  • Received : 2011.07.13
  • Accepted : 2011.08.26
  • Published : 2011.09.15
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Abstract

This study examined the bioaccumulation of the heavy metals copper (Cu) and zinc (Zn) by the giant kelp, Macrocystis pyrifera, by exposing meristematic kelp tissue to elevated metal concentrations in seawater within laboratory aquaria. Specifically, we carried out two different experiments. The first examined metal uptake under a single, ecologically-relevant elevation of each metal (30 ppb Cu and 100 ppb Zn), and the second examined the relationships between varying levels of the metals (i.e., 15, 39, 60, 120, 240, and 480 ppb Cu, and 50, 100, 200, 300, 500, and 600 ppb Zn). Both experiments were designed to contrast the uptake of the metals in isolation (i.e., when only one metal concentration was elevated) and in combination (i.e., when both metals' concentrations were elevated). Following three days of exposure to the elevated metal concentrations, we collected and analyzed the M. pyrifera tissues using inductively coupled plasma atomic emissions spectroscopy. Our results indicated that M. pyrifera bioaccumulated Cu in all treatments where Cu concentrations in the seawater were elevated, regardless of whether Zn concentrations were also elevated. Similarly, M. pyrifera bioaccumulated Zn in treatments where seawater Zn concentrations were elevated, but this occurred only when we increased Zn alone, and not when we simultaneously increased Cu concentrations. This suggests that elevated Cu concentrations inhibit Zn uptake, but not vice versa. Following this, our second experiment examined the relationships among varying seawater Cu and Zn concentrations and their bioaccumulation by M. pyrifera. Here, our results indicated that, as their concentrations in the seawater rise, Cu and Zn uptake by M. pyrifera tissue also rises. As with the first experiment, the presence of elevated Zn in the water did not appear to affect Cu uptake at any concentration examined. However, although it was not statistically significant, we observed that the presence of elevated Cu in seawater appeared to trend toward inhibiting Zn uptake, especially at higher levels of the metals. This study suggests that M. pyrifera may be useful as a bio-indicator species for monitoring heavy metal pollution in coastal environments.

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References

  1. Al-Homaidan, A. A. 2007. Heavy metal concentrations in three species of green algae from the Saudi coast of the Arabian Gulf. J. Food Agric. Environ. 5:354-358.
  2. Amado Filho, G. M., Karez, C. S., Andrade, L. R., Yoneshigue-Valentin, Y. & Pfeiffer, W. C. 1997. Effects on growth and accumulation of zinc in six seaweed species. Ecotoxicol. Environ. Saf. 37:223-228. https://doi.org/10.1006/eesa.1997.1541
  3. Anderson, B. S., Hunt, J. W., Turpen, S. L., Coulon, A. R. & Martin, M. 1990. Copper toxicity to microscopic stages of giant kelp Macrocystis pyrifera: interpopulation comparisons and temporal variability. Mar. Ecol. Prog. Ser. 68:147-156. https://doi.org/10.3354/meps068147
  4. Bates, S. S., Tessier, A., Campbell, P. G. C. & Buffle, J. 1982. Zinc adsorption and transport by Chlamydomonas varuiabilis and Scenedesmus subspicatus (Chlorophyceae) grown in semicontinuous culture. J. Phycol. 18:521-529. https://doi.org/10.1111/j.1529-8817.1982.tb03218.x
  5. Beckett, P. H. T. & Davis, R. D. 1978. The additivity of the toxic effects of Cu, Ni and Zn in young barley. New Phytol. 81:155-173. https://doi.org/10.1111/j.1469-8137.1978.tb01615.x
  6. Bird, P., Comber, S. D. W., Gardner, M. J. & Ravenscroft, J. E. 1996. Zinc inputs to coastal waters from sacrificial anodes. Sci. Total Environ. 181:257-264. https://doi.org/10.1016/0048-9697(95)05025-6
  7. Blossom, N. 2002. Session: copper for biofouling control. In Proc. 11th Int. Congr. Mar. Corrosion Fouling, San Diego, CA.
  8. Brown, R. J., Galloway, T. S., Lowe, D., Browne, M. A., Dissanayake, A., Jones, M. B. & Depledge, M. H. 2004. Differential sensitivity of three marine invertebrates to copper assessed using multiple biomarkers. Aquat. Toxicol. 66:267-278. https://doi.org/10.1016/j.aquatox.2003.10.001
  9. Bryan, G. W. 1969. The absorption of zinc and other metals by the brown seaweed Laminaria digitata. J. Mar. Biol. Assoc. U. K. 49:225-243. https://doi.org/10.1017/S0025315400046531
  10. Bryan, G. W. 1971. The effects of heavy metals (other than mercury) on marine and estuarine organisms. Proc. R. Soc. Lond. B Biol. Sci. 177:398-410.
  11. Connell, D. W. 1989. Biomagnification by aquatic organisms: a proposal. Chemosphere 19:1573-1584. https://doi.org/10.1016/0045-6535(89)90501-8
  12. Connell, D. W. 1990. Enviromental routes leading to the bioaccumulation of lipophilic chemicals. In Connell, D. W. (Ed.) Bioaccumulation of Xenobiotic Compounds. CRC Press, Boca Raton, FL, pp. 60-73.
  13. Conti, M. E. & Cecchetti, G. 2003. A biomonitoring study: trace metals in algae and molluscs from Tyrrhenian coastal areas. Environ. Res. 93:99-112. https://doi.org/10.1016/S0013-9351(03)00012-4
  14. Davis, T. A., Volesky, B. & Mucci, A. 2003. A review of the biochemistry of heavy metal biosorption by brown algae. Water Res. 37:4311-4330. https://doi.org/10.1016/S0043-1354(03)00293-8
  15. Deheyn, D. D. & Latz, M. I. 2006. Bioavailability of metals along a contamination gradient in San Diego Bay (California, USA). Chemosphere 63:818-834. https://doi.org/10.1016/j.chemosphere.2005.07.066
  16. Duffus, J. H. 2002. "Heavy metals": a meaningless term? Pure Appl. Chem. 74:793-807. https://doi.org/10.1351/pac200274050793
  17. Flegal, A. R. & Sanudo-Wilhelmy, S. A. 1993. Comparable levels of trace metal contamination in two semienclosed embayments: San Diego Bay and South San Francisco Bay. Environ. Sci. Technol. 7:1934-1936.
  18. Food and Nutrition Board. 2001. Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. National Academy Press, Washington, D. C., 773 pp.
  19. Foster, M. S. & Schiel, D. R .1985. The ecology of giant kelp forests in California: a community profile. U. S. Fish & Wildlife Service, Washington, D. C., 152 pp.
  20. Fu, J., Zhou, Q., Liu, J., Liu, W., Wang, T., Zhong, Q. & Jiang, G. 2008. High levels of heavy metals in rice (Oryza sativa L.) from a typical E-waste recycling area in southeast China and its potential risk to human health. Chemosphere 71:1269-1275. https://doi.org/10.1016/j.chemosphere.2007.11.065
  21. Fytianos, K., Evgenidou, E. & Zachariadis, G. 1999. Use of macroalgae as biological indicators of heavy metal pollution in Thermaikos Gulf, Greece. Bull. Environ. Contam. Toxicol. 62:630-637. https://doi.org/10.1007/s001289900921
  22. Gadd, G. M. 1988. Accumulation of metals by microorganisms and algae. In Rehm, H. J. & Reed, G. (Eds.) Biotechnology. VCH, Weinheim, pp. 401-434.
  23. Gaudry, A., Zeroual, S., Gaie-Levrel, F., Moskura, M., Boujrhal, F. -Z., El Moursli, R. C., Guessous, A., Mouradi, A., Givernaud, T. & Delmas, R. 2007. Heavy metals pollution of the atlantic marine environment by the Moroccan phosphate industry, as observed through their bioaccumulation in Ulva lactuca. Water Air Soil Pollut. 178:267-285. https://doi.org/10.1007/s11270-006-9196-9
  24. Graham, L. E. & Wilcox, L. W. 2000. Algae. Prentice-Hall, Inc. Upper Saddle River, NJ, 640 pp.
  25. Gray, J. S. 2002. Biomagnification in marine systems: the perspective of an ecologist. Mar. Pollut. Bull. 45:46-52. https://doi.org/10.1016/S0025-326X(01)00323-X
  26. Hall, A. 1980. Heavy metal co-tolerance in a copper-tolerant population of the marine fouling alga, Ectocarpus siliculosus (Dillw.) Lyngbye. New Phytol. 85:73-78. https://doi.org/10.1111/j.1469-8137.1980.tb04449.x
  27. Hamer, D. H. 1986. Metallothionein. Annu. Rev. Biochem. 55:913-951. https://doi.org/10.1146/annurev.bi.55.070186.004405
  28. Hebel, D. K., Jones, M. B. & Depledge, M. H. 1997. Responses of crustaceans to contaminant exposure: a holistic approach. Estuar. Coast. Shelf Sci. 44:177-184. https://doi.org/10.1006/ecss.1996.0209
  29. Huovinen, P., Leal, P. & Gomez, I. 2010. Interacting effects of copper, nitrogen and ultraviolet radiation on the physiology of three south Pacific kelps. Mar. Freshw. Res. 61:330-341. https://doi.org/10.1071/MF09054
  30. Jackson, G. A. & Winant, C. D. 1983. Effect of a kelp forest on coastal currents. Cont. Shelf Res. 2:75-80. https://doi.org/10.1016/0278-4343(83)90023-7
  31. Kadukova, J. & Vircikova, E. 2004. Comparison of differences between copper bioaccumulation and biosorption. Environ. Int. 31:227-232.
  32. Kimbrough, K. L., Johnson, W. E., Lauenstein, G. G., Christensen, J. D. & Apeti, D. A. 2008. An assessment of two decades of contaminant monitoring in the Nation's Coastal Zone. NOAA Technical Memorandum NOS NCCOS 74. National Oceanic and Atmospheric Centers for Coastal Ocean Science, Center for Coastal Monitoring and Assessment, Silver Spring, MD, 105 pp.
  33. Krzeslowska, M. 2011. The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol. Plant. 33:35-51. https://doi.org/10.1007/s11738-010-0581-z
  34. Lenihan, H. S., Peterson, C. H., Kim, S. L., Conlan, K. E., Fairey, R., McDonald, C., Grabowski, J. H. & Oliver, J. S. 2003. Variation in marine benthic community composition allows discrimination of multiple stressors. Mar. Ecol. Prog. Ser. 261:63-73. https://doi.org/10.3354/meps261063
  35. Levitt, J. 1980. Responses of plants to environmental stresses. Vol. 2. 2nd ed. Academic Press, New York, NY, 698 pp.
  36. Liu, X. -J., Ni, I. -H. & Wang, W. -X. 2002. Trophic transfer of heavy metals from freshwater zooplankton Daphnia magna to zebrafish Danio reiro. Water Res. 36:4563-4569. https://doi.org/10.1016/S0043-1354(02)00180-X
  37. Luo, Y. & Rimmer, D. L. 1995. Zinc-copper interaction affecting plant growth on a metal-contaminated soil. Environ. Pollut. 88:79-83. https://doi.org/10.1016/0269-7491(95)91050-U
  38. Manahan, S. E. 1991. Environmental chemistry. Lewis Publishers, Chelsea, MI, 583 pp.
  39. Martin, M. H. & Coughtrey, P. J. 1982. Biological monitoring of heavy metal pollution: land and air. Applied Science Publishers, London and New York, 475 pp.
  40. Mehta, S. K. & Gaur, J. P. 2005. Use of algae for removing heavy metal ions from wastewater: progress and prospects. Crit. Rev. Biotechnol. 25:113-152. https://doi.org/10.1080/07388550500248571
  41. Naimo, T. J. 1995. A review of the effects of heavy metals on freshwater mussels. Ecotoxicology 4:341-362. https://doi.org/10.1007/BF00118870
  42. Pellegrini, M., Laugier, A., Sergent, M., Phan-Tan-Luu, R., Valls, R. & Pellegrini, L. 1993. Interactions between the toxicity of the heavy metals cadmium, copper, zinc in combinations and the detoxifying role of calcium in the brown alga Cystoseira barbata. J. Appl. Phycol. 5:351-361. https://doi.org/10.1007/BF02186238
  43. Phillips, D. J. H. 1976. The common mussel Mytilus edulis as an indicator of pollution by zinc, cadmium, lead and copper. I. Effects of environmental variables on uptake of metals. Mar. Biol. 38:59-69. https://doi.org/10.1007/BF00391486
  44. Rai, L. C., Gaur, J. P. & Kumar, H. D. 1981. Phycology and heavy metal pollution. Biol. Rev. 56:99-151.
  45. Rai, L. C., Kumar, H. D., Mohn, F. H. & Soeder, C. J. 2000. Services of algae to the enviroment. J. Microbiol. Biotechnol. 10:119-136.
  46. Rainbow, P. S. 1995. Biomonitoring of heavy metal avalability in the marine environment. Mar. Pollut. Bull. 31:183-192. https://doi.org/10.1016/0025-326X(95)00116-5
  47. Rainbow, P. S. 2002. Trace metal concentrations in aquatic invertebrates: why and so what? Environ. Pollut. 120:497-507. https://doi.org/10.1016/S0269-7491(02)00238-5
  48. Rainbow, P. S. 2007. Trace metal bioaccumulation: models, metabolic availability and toxicity. Environ. Int. 33:576-582. https://doi.org/10.1016/j.envint.2006.05.007
  49. Rainbow, P. S. & White, S. L. 1989. Comparative strategies of heavy metal accumulation by crustaceans: zinc, copper and cadmium in a decapod, and amphipod and a barnacle. Hydrobiologia 174:245-262. https://doi.org/10.1007/BF00008164
  50. Rand, G. M, Wells, P. G. & McCarthy, L. S. 1995. Introduction to aquatic ecology. In Rand, G. M. (Ed.) Fundamentals of Aquatic Toxicology: Effects, Environmental Fate and Risk Assessment. Taylor and Francis, London, pp. 3-53.
  51. Ratte, H. T. 1999. Bioaccumulation and toxicity of silver compounds: a review. Environ. Toxicol. Chem. 18:89-108. https://doi.org/10.1002/etc.5620180112
  52. Reed, R. H. & Gadd, G. M. 1989. Metal tolerance in eukaryotic and prokaryotic algae. In Shaw, J. A. (Ed.) Heavy Metal Tolerance in Plants: Evolutionary Aspects. CRC Press, Boca Raton, FL, pp. 105-118.
  53. Reinfelder, J. R., Fisher, N. S., Luoma, S. N., Nichols, J. W. & Wang, W. -X. 1998. Trace element trophic transfer in aquatic organisms: a critique of the kinetic model approach. Sci. Total Environ. 219:117-135. https://doi.org/10.1016/S0048-9697(98)00225-3
  54. San Diego Port District. 2009. The big bay San Diego Bay. Available from: http://www.harborislandwest.com/. Accessed Mar. 22, 2009.
  55. Schiff, K., Bay, S. & Diehl, D. 2001. Stormwater toxicity in Chollas Creek and San Diego Bay, California. Environ. Monit. Assess. 81:119-132.
  56. Smith, P. G. & Scott, J. S. 1981. Dictionary of water and waste treatment. Elsevier Butterworths-Heinemann, London, 486 pp.
  57. Storelli, M. M., Storelli, A. & Marcotrigiano, G. O. 2001. Heavy metals in the aquatic envrionment of the Southern Adriatic Sea, Italy: macroalgae, sediments and benthic species. Envrion. Int. 26:505-509. https://doi.org/10.1016/S0160-4120(01)00034-4
  58. Stromgren, T. 1980. The effects of dissolved copper on the increase in length of four species of intetidal fucoid algae. Mar. Envrion. Res. 3:5-13. https://doi.org/10.1016/0141-1136(80)90032-X
  59. Verkleij, J. A. C. & Schat, H. 1989. Mechanisms of metal tolerance in higher plants. In Shaw, A. J. (Ed.) Heavy Metal Tolerance in Plants: Evolutionary Aspects. CRC Press, Boca Raton, FL, pp. 179-193.
  60. Volpe, A. M. & Esser, B. K. 2002. Real-time ocean chemistry for improved biogeochemical observation in dynamic coastal environments. J. Mar. Syst. 36:51-74. https://doi.org/10.1016/S0924-7963(02)00125-2
  61. Warnau, M., Ledent, G., Temara, A., Jangoux, M. & Dubois, P. 1995. Experimental cadmium contamination of the echinoid Paracentrotus lividus: influence of exposure mode and distribution of the metal in the organism. Mar. Ecol. Prog. Ser. 116:117-124. https://doi.org/10.3354/meps116117

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