Metal accumulation and impacts in phytoplankton

  • James G. Sanders
  • Gerhardt F. Riedel


This chapter examines processes that regulate and influence trace element uptake, accumulation, transformation, release and toxicity in natural aquatic systems. Phytoplankton are efficient accumulators of most reactive elements. Many inorganic compounds, including most metals, are involved in the oxidative and reductive reactions that comprise cellular metabolism. Some elements are required in small quantities but are toxic in larger quantities. Although materials associated with phytoplankton behave in a manner somewhat similar to particulates, incorporation of a toxic compound markedly affects the compound’s transport through aquatic ecosystems. Toxic com-pounds may also pass to successively higher trophic levels through interactions between predators and their prey.


Metal Accumulation High Trophic Level Marine Ecology Progress Series Marine Phytoplankton Phaeodactylum Tricornutum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ahner, B.A. and Morel, F.M.M. (1995) Phytochelatin production in marine algae. 2. Induction by various metals. Limnology and Oceanography 40, 658–665.CrossRefGoogle Scholar
  2. Ahner, B.A., Price, N. and Morel, F.M.M. (1994) Phytochelatin production by marine phytoplankton at low free metal ion concentrations: laboratory studies and field data from Massachusetts Bay. Proceedings of the National Academy of Sciences, USA 91, 8433–8436.CrossRefGoogle Scholar
  3. Ahner, B.A., Kong, S. and Morel, F.M.M. (1995) Phytochelatin production in marine algae. 1. An interspecies comparison. Limnology and Oceanography 40, 649–657.CrossRefGoogle Scholar
  4. Anderson, D.M. and Morel, F.M.M. (1978) Copper sensitivity of Gonyaulax tamarensis. Limnology and Oceanography 23, 283–295.CrossRefGoogle Scholar
  5. Andreae, M.O. and Froelich, P.N. (1984) Arsenic, antimony and germanium biogeo-chemistry in the Baltic Sea. Tellus 36B, 101–117.CrossRefGoogle Scholar
  6. Azam, F., Hemmingsne, B.B. and Volcani, B.J. (1973) Germanium incorporation into the silica of diatom cell walls. Archiv für Mikrobiologie 92, 11–20.CrossRefGoogle Scholar
  7. Berland, B.R., Bonin, D.J., Guérin-Ancey, O.J. et al. (1977) Action de métaux lourds à des doses sublétales sur les caractéristiques de la croissance chez la diatomée Skeletonema costatum. Marine Biology 42, 17–30.CrossRefGoogle Scholar
  8. Besser, J.M., Huckins, J.N. and Clark, R.C. (1994) Separation of selenium species released from Se-exposed algae. Chemosphere 29, 771–780.CrossRefGoogle Scholar
  9. Blum, J.J. (1966) Phosphate uptake by phosphate-starved Euglena. Journal of General Physiology 49, 1125–1136.CrossRefGoogle Scholar
  10. Braek, G.S., Maines, D. and Jensen, A. (1980) Heavy metal tolerance of marine phytoplankton. IV. Combined effect of zinc and cadmium on growth and uptake in some marine diatoms. Journal of Experimental Marine Biology and Ecology 42, 39–54.CrossRefGoogle Scholar
  11. Brand, L.E., Sunda, W.G. and Guillard, R.R.L. (1986) Reduction of marine phytoplankton reproduction rates by copper and cadmium. Journal of Experimental Marine Biology and Ecology 96, 225–250.CrossRefGoogle Scholar
  12. Brockmann, U. and Dahl, E. (1990) Distribution of organic compounds during a bloom of Chrysochromulina polylepis in the Skagerrak, in Toxic Marine Phytoplankton, (eds E. Granelli, B. Sundstrom, L. Edler, and D.M. Anderson), Elsevier, New York, pp. 104–109.Google Scholar
  13. Bruland, K.W. (1989) Complexation of zinc by natural organic ligands in the central North Pacific. Limnology and Oceanography 34, 269–285.CrossRefGoogle Scholar
  14. Bruland, K.W. (1992) Complexation of cadmium by natural organic ligands in the central North Pacific. Limnology and Oceanography 37, 1008–1017.CrossRefGoogle Scholar
  15. Coale, K.H. and Bruland, K.W. (1988) Copper complexation in the northeast Pacific. Limnology and Oceanography 33, 1084–1101.CrossRefGoogle Scholar
  16. Connell, D.B., Sanders, J.G., Riedel, G.F. and Abbe, G.R. (1991) Pathways of silver uptake and trophic transfer in estuarine organisms. Environmental Science and Technology 25, 921–924.CrossRefGoogle Scholar
  17. Cooke, T.D. and Bruland, K.W. (1987) Aquatic chemistry of selenium: evidence of biomethylation. Environmental Science and Technology 21, 1214–1219.CrossRefGoogle Scholar
  18. Davis, CO. (1982) The importance of understanding phytoplankton life strategies in the design of enclosure experiments, in Marine Mesocosms, (eds G.D. Grice and M.R. Reeve), Springer-Verlag, New York, pp. 323–332.CrossRefGoogle Scholar
  19. Donat, J.R., Lao, K.A. and Bruland, K.W. (1994) Speciation of dissolved copper and nickel in South San Francisco Bay: a multi-method approach. Analytica Chimica Acta 284, 547–571.CrossRefGoogle Scholar
  20. Dzombak, D.A., Fish, W. and Morel, F.M.M. (1986) Metal-humate interactions. 1. Discrete ligand and continuous distribution models. Environmental Science and Technology 20, 669–675.CrossRefGoogle Scholar
  21. Fisher, N.S. (1986) On the reactivity of metals for marine phytoplankton. Limnology and Oceanography 31, 443–449.CrossRefGoogle Scholar
  22. Fisher, N.S. and Fabris, J.G. (1982) Complexation of Cu, Zn, and Cd by metabolites excreted from marine diatoms. Marine Chemistry 11, 245–255.CrossRefGoogle Scholar
  23. Fisher, N.S. and Wente, M. (1993) Release of trace elements by dying marine phyto-plankton. Deep-Sea Research 40, 671–694.CrossRefGoogle Scholar
  24. Fisher, N.S., Bohé, M. and Teyssié, J.-L. (1984) Accumulation and toxicity of Cd, Zn, Ag, and Hg in four marine phytoplankters. Marine Ecology Progress Series 18, 201–213.CrossRefGoogle Scholar
  25. Foe, C. and Knight, A.W. (1986) Selenium bioaccumulation, regulation, and toxicity in the green alga, Selenastrum capricornutum, and dietary toxicity of contaminated alga to Daphnia magna, in Selenium in the Environment, (ed. L.J. Slocum), California State University, Fresno, pp. 77–88.Google Scholar
  26. Foster, P.L. and Morel, F.M. (1982) Reversal of cadmium toxicity in a diatom: an interaction between cadmium activity and iron. Limnology and Oceanography 27,745–751.CrossRefGoogle Scholar
  27. Froelich, P.N., Daul, L.W., Byrd, J.T. et al. (1985) Arsenic, barium, germanium, tin, dimethylsulfide and nutrient biogeochemistry in Charlotte Harbor, Florida, a phosphorus-enriched estuary. Estuarine, Coastal and Shelf Science 20, 239–264.CrossRefGoogle Scholar
  28. Gavis, J., Guillard, R.R.L. and Woodward, B.L. (1981) Cupric ion activity and the growth of phytoplankton clones isolated from different marine environments. Journal of Marine Research 39, 315–333.Google Scholar
  29. Gekeler, W., Grill, E., Winnacker, E.-L. and Zenk, M.H. (1988) Algae sequester heavy metals via synthesis of phytochelatin complexes. Arch. Microbiol. 150, 197–202.CrossRefGoogle Scholar
  30. Gordon, A.S., Dyer, B.J., Kango, R.A. and Donat, J.R. (1996) Copper ligands isolated from estuarine water by immobilized metal affinity chromatography: temporal variability and partial characterization. Marine Chemistry 53, 163–172.CrossRefGoogle Scholar
  31. Gustavson, K. and Wangberg, S.-A. (1995) Tolerance induction and succession in microalgae communities exposed to copper and atrazine. Aquatic Toxicology 32, 283–302.CrossRefGoogle Scholar
  32. Gutknecht, J. (1981) Inorganic mercury (Hg2+) transport through lipid bilayer membranes. Journal of Membrane Biology 61, 61–66.CrossRefGoogle Scholar
  33. Harrison, W.G., Eppley, R.W. and Renger, E.H. (1977) Phytoplankton nitrogen metabolism, nitrogen budgets, and observations on copper toxicity: controlled ecosystem pollution experiment. Bulletin of Marine Science 27, 44–57.Google Scholar
  34. Howard, A.G., Arbab-Zavar, M.H. and Apte, S.C. (1982) Seasonal variability of bio-logical arsenic methylation in the estuary of the river Beaulieu. Marine Chemistry 11, 493–498.CrossRefGoogle Scholar
  35. Howard, A.G., Arbab-Zavar, M.H. and Apte, S.C. (1984) The behaviour of dissolved arsenic in the estuary of the river Beaulieu. Estuarine, Coastal and Shelf Science 19, 493–504.CrossRefGoogle Scholar
  36. Howard, A.G., Apte, S.C., Comber, S.D.W. and Morris, R.J. (1988) Biogeochemical control of the summer distribution and speciation of arsenic in the Tamar estuary. Estuarine, Coastal and Shelf Science 27, 427–444.CrossRefGoogle Scholar
  37. Kayser, H. (1982) Cadmium effects in food chain experiments with marine plankton algae (Dinophyta) and benthic filter feeders (Tunicata). Netherlands Journal of Sea Research 16, 444–454.CrossRefGoogle Scholar
  38. Kayser, H. and Sperling, K.R. (1980) Cadmium effects and accumulation in cultures of Prorocentrum micans (Dinophyta). Helgolander Meeresuntersuchungen 33, 89–102.CrossRefGoogle Scholar
  39. Kiffney, P. and Knight, A. (1990) The toxicity and bioaccumulation of selenate, selenite, and seleno-L-methionine in the cyanobacterium Anabaena flos-aquae. Archives of Environmental Contamination and Toxicology 19, 488–494.CrossRefGoogle Scholar
  40. Knowles, F.C. (1982) The enzyme inhibitory form of inorganic arsenic. Biochemistry International 4, 647–653.Google Scholar
  41. Knowles, F.C. and Benson, A.A. (1983) The biochemistry of arsenic. Trends in Biochemical Science 8, 178–180.CrossRefGoogle Scholar
  42. Kumar, H.K. and Prakish, G. (1971) Toxicity of selenium to the blue-green algae Anacystis nidulans said Anabaena variabilis. Annals of Botany 35, 697–705.Google Scholar
  43. Lee, B.-G. and Fisher, N.S. (1992) Degradation and elemental release rates from phy-toplankton debris and their geochemical implications. Limnology and Oceanography 37, 1345–1360.CrossRefGoogle Scholar
  44. Lee, B.-G. and Fisher, N.S. (1994) Effects of sinking and zooplankton grazing on release of elements from planktonic debris. Marine Ecology Progress Series 110, 271–281.CrossRefGoogle Scholar
  45. Lee, J.G., Ahner, B.A. and Morel, F.M.M. (1996) Export of cadmium and phy-tochelatin by the marine diatom Thalassiosira weissflogii. Environmental Science and Technology 30, 1814–1821.CrossRefGoogle Scholar
  46. Li, W.K.W. (1978) Kinetic analysis of interactive effects of cadmium and nitrate on growth of Thalassiosira fluviatilis (Bacillariophyceae). Journal of Phycology 14, 454–460.CrossRefGoogle Scholar
  47. Margalef, R. (1962) Succession in marine populations. Advancing Frontiers of Plant Sciences New Delhi, 2, 137–188.Google Scholar
  48. McKnight, D.M. and Morel, F.M.M. (1979) Release of weak and strong copper-com-plexing agents by algae. Limnology and Oceanography 24, 823–837.CrossRefGoogle Scholar
  49. Moffett, J.W. and Brand, L.E. (1996) Production of strong, extracellular Cu chelators by marine cyanobacteria in response to Cu stress. Limnology and Oceanography 41, 388–395.CrossRefGoogle Scholar
  50. Moffett, J.W., Zika, R.G. and Brand, L.E. (1990) Distribution and potential sources and sinks of copper chelators in the Sargasso Sea. Deep-Sea Research 37, 27–36.CrossRefGoogle Scholar
  51. Morel, F.M.M., Hudson, R.J.M. and Price, N.M. (1991) Limitation of productivity by trace metals in the sea. Limnology and Oceanography 36, 1742–1755.CrossRefGoogle Scholar
  52. Morel, N.M., Rueter, J.E. and Morel, F.M.M. (1978) Copper toxicity to Skeletonema costatum. Journal of Phycology 14, 43–48.CrossRefGoogle Scholar
  53. Morrelli, E. and Scarano, G. (1995) Cadmium induced phytochelatins in marine alga Phaeodactylum tricornutum: effect of metal speciation. Chemical Speciation and Bioavailability 7, 43–47.Google Scholar
  54. Oliviera, R. (1985) Phytoplankton communities response to a mine effluent rich in copper. Hydrobiologia 128, 61–69.CrossRefGoogle Scholar
  55. Peoples, S.A. (1975) Review of arsenical pesticides, in Arsenical Pesticides, (ed. E.A. Woolson), American Chemical Society, Washington, DC, pp. 1–12.CrossRefGoogle Scholar
  56. Phinney, J.T. and Bruland, K.W. (1994) Uptake of lipophilic organic Cu, Cd, and Pb complexes in the coastal diatom Thalassiosira weissflogii. Environmental Science and Technology 28, 1781–1817.CrossRefGoogle Scholar
  57. Planas, D. and Healey, F.P. (1978) Effects of arsenate on growth and phosphorus metabolism of phytoplankton. Journal of Phycology 14, 337–341.CrossRefGoogle Scholar
  58. Reinfelder, J.R. and Fisher, N.S. (1991) The assimilation of elements ingested by marine copepods. Science 251, 794–796.CrossRefGoogle Scholar
  59. Reinfelder, J.R. and Fisher, N.S. (1994) The assimilation of elements ingested by marine planktonic larvae. Limnology and Oceanography 39, 12–20.CrossRefGoogle Scholar
  60. Riedel, G.F. (1984) Influence of salinity and sulfate on the toxicity of chromium (VI) to the estuarine diatom Thalassiosira pseudonana. Journal of Phycology 20, 496–500.CrossRefGoogle Scholar
  61. Riedel, G.F. (1985) The relationship between chromium(VI) uptake, sulfate uptake, and chromium(VI) toxicity in the estuarine diatom, Thalassiosira pseudonana. Aquatic Toxicology 7, 191–204.CrossRefGoogle Scholar
  62. Riedel, G.F. (1988) Interspecific and geographic variation of the chromium sensitivity of algae, in Proceedings, 11th Symposium on Aquatic Toxicology and Hazard Assessment, (eds G.W. Suter and M. Lewis), American Society of Testing and Materials, Philadelphia, pp. 537–548.Google Scholar
  63. Riedel, G.F. and Sanders, J.G. (1996) The influence of pH and media composition on the uptake of inorganic selenium by Chlamydomonas reinhardtii. Environmental Toxicology and Chemistry 15, 1577–1583.Google Scholar
  64. Riedel, G.F., Sanders, J.G. and Gilmour, C.C. (1996) Uptake, transformation, and impact of selenium in freshwater phytoplankton and bacterioplankton communities. Aquatic Microbiology and Ecology 11, 43–51.CrossRefGoogle Scholar
  65. Sanders, J.G. (1979) Effects of arsenic speciation and phosphate concentration on arsenic inhibition of Skeletonema costatum (Bacillariophyceae). Journal of Phycology 15, 424–428.Google Scholar
  66. Sanders, J.G. (1980) Arsenic cycling in marine systems. Marine Environmental Research 3, 257–266.CrossRefGoogle Scholar
  67. Sanders, J.G. (1985) Arsenic geochemistry in Chesapeake Bay: dependence upon anthropogenic inputs and phytoplankton species composition. Marine Chemistry 17, 328–340.CrossRefGoogle Scholar
  68. Sanders, J.G. and Abbe, G.R. (1987) The role of suspended sediments and phytoplankton in the partitioning and transport of silver in estuaries. Continental Shelf Research, 1357–1361.Google Scholar
  69. Sanders, J.G. and Abbe, G.R. (1989) Silver transport and impact in estuarine and marine systems, in Aquatic Toxicology and Environmental Fate, Vol. 11, (eds G. Suter and M. Lewis), American Society for Testing and Materials STP 1007, Philadelphia, pp. 5–18.Google Scholar
  70. Sanders, J.G. and Cibik, S.J. (1985a) Adaptive behavior of euryhaline phytoplankton communities to arsenic stress. Marine Ecology Progress Series 22, 199–205.CrossRefGoogle Scholar
  71. Sanders, J.G. and Cibik, S.J. (1985b) Reduction of growth rate and resting spore formation in a marine diatom exposed to low levels of cadmium. Marine Environmental Research 16, 165–180.CrossRefGoogle Scholar
  72. Sanders, J.G. and Riedel, G.F. (1987) Control of trace element toxicity by phytoplankton, in Recent Advances in Phytochemistry, Vol. 21, (eds J. A. Saunders, L. Kosak-Channing and E.E. Conn), Plenum Press, New York, pp. 131–149.Google Scholar
  73. Sanders, J.G. and Riedel, G.F. (1993) Trace element transformation during the devel-opment of an estuarine algal bloom. Estuaries 16, 521–532.CrossRefGoogle Scholar
  74. Sanders, J.G. and Vermersch, P.S. (1982) Response of marine phytoplankton to low levels of arsenate. Journal of Plankton Research 4, 881–893.CrossRefGoogle Scholar
  75. Sanders, J.G. and Windom, H.L. (1980) The uptake and reduction of arsenic species by marine algae. Estuarine and Coastal Marine Science 10, 555–567.CrossRefGoogle Scholar
  76. Sanders, J.G., Ryther, J.H. and Batchelder, J.H. (1981) Effects of copper, chlorine, and thermal addition on the species composition of marine phytoplankton. Journal of Experimental Marine Biology and Ecology 49, 81–102.CrossRefGoogle Scholar
  77. Sanders, J.G., Osman, R.W. and Riedel, G.F. (1989) Pathways of arsenic uptake and incorporation in estuarine phytoplankton and filter-feeding invertebrates, Eurytemora affinis, Balanus improvisus, and Crassostrea virginica. Marine Biology 103, 319–325.CrossRefGoogle Scholar
  78. Sanders, J.G., Riedel, G.F. and Ferrier, D.P. (1991) Changes in community structure of Chesapeake Bay phytoplankton when exposed to low levels of trace metals: management implications, in New Perspectives in the Chesapeake System: A Research and Management Partnership, (eds J.A. Mihursky and A. Chaney), Proceedings of a Conference 4–6 December 1990, Baltimore, MD, Chesapeake Research Consortium Publication No. 137, pp. 451–460.Google Scholar
  79. Sanders, J.G., Riedel, G.F. and Osman, R.W. (1994). Arsenic cycling and impact in estuarine and coastal marine ecosystems, in Arsenic in the Environment, Part I: Cycling and Characterization, (ed. J.O. Nriagu), John Wiley and Sons, New York, pp. 289–308.Google Scholar
  80. Schindler, D.W. (1987) Detecting ecosystem response to anthropogenic stress. Canadian Journal of Fisheries and Aquatic Sciences 44 (Suppl. 1), 6–25.CrossRefGoogle Scholar
  81. Sharp, J.H. (1977) Excretion of organic matter by marine phytoplankton: do healthy cells do it? Limnology and Oceanography 22, 381–399.CrossRefGoogle Scholar
  82. Sick, L.V. and Windom, H.L.(1975) Effects of environmental levels of mercury and cadmium on rates of metal uptake and growth physiology of selected genera of marine phytoplankton, in Mineral Cycling in Southeastern Ecosystems, (eds F.G. Howell, J.B. Gentry and M.H. Smith), CONF-740513, NTIS, Springfield, VA, pp. 239–249.Google Scholar
  83. Sunda, W.G. (1988/89) Trace metal interactions with marine phytoplankton. Biological Oceanography 6, 411–442.Google Scholar
  84. Sunda, W.G. (1994) Trace metal/phytoplankton interactions in the sea, in Chemistry of Aquatic Systems: Local and Global Perspectives, (eds G. Bidoglio and W. Stumm),ECSC, EEC, EAEC, Brussels and Luxembourg, pp. 213–247.Google Scholar
  85. Sunda, W.G. and Guillard, R.R.L. (1976) The relationship between cupric activity and the toxicity of copper to phytoplankton. Journal of Marine Research 34, 511–529.Google Scholar
  86. Thomas, W.H., Holm-Hansen, O., Seibert, D.L.R. et al (1977) Effects of copper on phytoplankton standing crop and productivity: controlled ecosystem pollution experiment. Bulletin of Marine Science 27, 34–43.Google Scholar
  87. Trick, C.G., Andersen, R.J., Price, N.M. et al. (1983) Examination of hydroxamate-siderophore production by neritic eukaryotic marine phytoplankton. Marine Biology 75, 9–17.CrossRefGoogle Scholar
  88. Wangersky, P.J., Bradley Moran, S., Pett, R.J. et al (1989) Biological control of trace metal residence times: An experimental approach. Marine Chemistry 28, 215–226.CrossRefGoogle Scholar
  89. Wheeler, A.E., Zingaro, R.A. and Irgolic, K. (1982) The effect of selenate, selenite and sulfate on six species of unicellular algae. Journal of Experimental Marine Biology and Ecology 57, 181–194.CrossRefGoogle Scholar
  90. Wilhelm, S.W. and Trick, C.G. (1994) Iron-limited growth of cyanobacteria: multiple siderophore production is a common response Limnology and Oceanography 39, 1979–1984.CrossRefGoogle Scholar
  91. Wilhelm, S.W., Maxwell, D.P. and Trick, C.G. (1996) Growth, iron requirements, and siderophore production in iron-limited Synechococcus PCC 7002. Limnology and Oceanography 41, 89–97.CrossRefGoogle Scholar
  92. Winner, R.W. and Owen, H.A. (1991) Seasonal variability in the sensitivity of freshwater phytoplankton ommunities to a chronic copper stress. Aquatic Toxicology 19, 73–88.CrossRefGoogle Scholar
  93. Wrench, J.J. (1978) Selenium metabolism in the marine phytoplankton Tetraselmis tetrathele and Dunaliella minuta. Marine Biology 49, 231–236.CrossRefGoogle Scholar
  94. Zhou, X. and Wangersky, P.J. (1989) Production of copper-complexing organic lig-ands by the marine diatom Phaeodactylum tricornutum in a cage culture tur-bidostat. Marine Chemistry 26, 239–259.CrossRefGoogle Scholar
  95. Zhou, X., Slauenwhite, D.E., Pett, R.J. and Wangersky, P.J. (1989) Production of cop-per-complexing organic ligands during a diatom bloom: Tower tank and batch culture experiments. Marine Chemistry 27, 19–30.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1998

Authors and Affiliations

  • James G. Sanders
  • Gerhardt F. Riedel

There are no affiliations available

Personalised recommendations