Water, Air and Soil Pollution: Focus

, Volume 3, Issue 1, pp 7–26 | Cite as

Macroalgal growth in nutrient-enriched estuaries: A biogeochemical and evolutionary perspective

  • John A. Raven
  • Rebecca Taylor


Increased nutrient loading of a body of water leads to an increase in macroalgal growth. It is generally observed, however, that certain species thrive more than others, capitalising on the increased nutrient availability. These are usually small, fast-growing, ephemeral algae that often appear as nuisance blooms. This article discusses the correlation between nutrient increase and macroalgal bloom formation. From a historical perspective, the evolutionary history of nuisance macroalgae, and the habits available to them prior to anthropogenic influences on estuarine geochemistry are considered. The occurrence of macroalgal genera whose distribution is commonly related to estuaries with high nutrient loading is discussed, along with evidence suggesting that the ecophysiological traits of r-selected, ephemeral algae largely contribute to their ecological success and bloom-formation at nutrient-enriched sites.

ecophysiology estuaries growth life strategy macroalgal blooms morphology -nutrients uptake rate 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Algeo, T. J. and Sheckler, S. E.: 1998, 'Terrestrial-marine teleconnections in the Devonian: Links between the evolution of land plants, weathering processes, and marine anoxic events', Phil. Trans. Roy. Soc. Lond. B 353, 113–30.Google Scholar
  2. Amat, M. A. and Braud, J-P.: 1990, 'Ammonium uptake by Chondrus crispus Stackhouse (Gigartinales: Rhodophyta) in culture', Hydrobiologia 204/205, 467–471.Google Scholar
  3. Antia, N. H., Harrison P. J. and Oliveira L.: 1991, 'The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology', Phycologia 30, 1–89.Google Scholar
  4. Aubert, M.: 1990, 'Summer time proliferation of toxic plankton', Recherche 21, 916–919.Google Scholar
  5. Benton, M. J.: 2000, Vertebrate Palaeontology, Second Edition, Blackwell Science, Oxford, U.K.Google Scholar
  6. Bischoff, B. and Wiencke, C.: 1993, 'Temperature requirements for growth and survival of macroalgae from Disko Island (Greenland)', Helgolander wiss. Meeresunters. 47, 167–191.Google Scholar
  7. Blomster, J., Stanhope, M. J. and Maggs, C. A.: 1998, 'Molecular and morphogenetic analysis of Enteromorpha intestinalis and E. compressa (Chlorophyta) in the British Isles', J. Phycol. 34, 319–40.Google Scholar
  8. Carpenter, R. C.: 1990, 'Competition among marine macroalgae: A physiological perspective',J. Phycol. 26, 6–12.Google Scholar
  9. Cohen, I. and Neori, A.: 1991, 'Ulva lactuca biofilters for marine fishpond effluents', Bot. Mar. 34, 475–482.Google Scholar
  10. Dayton, P. K.: 1975, 'Experimental evaluation of ecological dominance in a rocky intertidal algal community', Ecol. Monogr. 45, 137–158.Google Scholar
  11. DeBoer, J. A.: 1981, 'Nutrients', in C. S. Lobban and M. J. Wynne (eds.), The Biology of Seaweeds, Botanical Monographs, Vol. 17, Blackwell Scientific Publications, Oxford, U.K, pp. 356–392.Google Scholar
  12. D'Elia, D. F. and DeBoer, J. A.: 1978, 'Nutritional studies of two red algae. II. Kinetics of ammonium and nitrate uptake',J. Phycol. 14, 266–272.Google Scholar
  13. DeVries, I., Philippart, C. J. M., De Groot, E. G. and van der Toll, M. W. M.: 1996, 'Coastal eutrophication and marine benthic vegetation: A model analysis', in W. Schramm and P. Neinhuis (eds.), Ecological Studies, Vol. 123. Marine Benthic Vegetation: Recent Changes and the Effects of Eutrophication, Springer-Verlag, Berlin, pp. 79–114.Google Scholar
  14. Dodds, K. D. and Gudder, D. A.: 1992, 'The ecology of Cladophora',J. Phycol. 28, 415–427.Google Scholar
  15. Downhower, J. F. and Blumer, L. S.: 1988, 'Calculating just how small a whale can be', Nature 335, 675.Google Scholar
  16. Downhower, J. F. and Blumer, L. S.: 1989, 'Size of aquatic endotherms', Nature 341, 192.Google Scholar
  17. Duke, C. S., Litaker, W. and Ramus, J.: 1989, 'Effects of the temperature, nitrogen supply and tissue nitrogen on ammonium uptake rates of the Chlorophyte seaweeds Ulva curvata and Codium decorticatum',J. Phycol. 25, 113–120.Google Scholar
  18. Edwards, P.: 1972, 'Cultured red alga to measure pollution', Mar. Pollut. Bull. 3, 184–188.Google Scholar
  19. Edwards, P.: 1973, 'The benthic marine algae of polluted estuaries on County Durham', Proc. Challenger Soc. 4, 161–162.Google Scholar
  20. Fahy, E., Goodwillie, R., Rochford, J. and Kelly, D.: 1975, 'Eutrophication of a partially enclosed estuarine mudflat', Mar. Pollut. Bull. 6, 29–31.Google Scholar
  21. Falkowski, P. G. and Raven, J. A.: 1997, Aquatic Photosynthesis, Blackwell Science, Malden, Mass.Google Scholar
  22. Fitzgerald, W. J.: 1978, 'Environmental parameters influencing the growth of Enteromorpha clathrata (Roth). J. Ag. in the intertidal zone in Guam', Bot. Mar. 21, 207–220.Google Scholar
  23. Fletcher, R. L.: 1996, 'The occurrence of “Green Tides” - a review', in W. Schramm and P. Neinhuis (eds.), Ecological Studies, Vol. 123. Marine Benthic Vegetation, Springer-Verlag, Berlin Heidelberg, pp. 7–43.Google Scholar
  24. Fortes, M. D. and Lüning, K.: 1980, 'Growth rates of North Sea macroalgae in relation to temperature, irradiance and photoperiod', Helgolander wiss. Meeresunters. 34, 15–29.Google Scholar
  25. Fujita, R. M., Wheeler, P. A. and Edwards, R. L.: 1988, 'Metabolic regulation of ammonium uptake by Ulva rigida (Chlorophyta): A compartmental analysis of the rate-limiting step for uptake',J. Phycol. 24, 560–566.Google Scholar
  26. Fujita, R. M.: 1985, 'The role of nitrogen status in regulating transient ammonium uptake and nitrogen storage by macroalgae', J. Exp. Mar. Biol. Ecol. 92, 283–301.Google Scholar
  27. Gavis, J.: 1976, 'Munk and Riley revisited: Nutrient diffusion transport and rates of phytoplankton growth', J. Mar. Res. 34, 161–179.Google Scholar
  28. Geertz-Hansen, O., Sand-Jensen, K., Hansen, D. F. and Christiansen, A.: 1993, 'Growth and grazing control of abundance of the marine macroalga Ulva lactuca L. in a eutrophic Danish estuary', Aquat. Bot. 46, 101–109.Google Scholar
  29. Gordon, D. M., Birch, P. B. and McComb, A. J.: 1980, 'The effect of light, temperature and salinity on photosynthetic rates of an estuarine Cladophora', Bot. Mar. 23, 749–755.Google Scholar
  30. Gordon, D. M., Birch, P. B. and McComb, A. J.: 1981, 'Effects of inorganic phosphorus and nitrogen on the growth of an estuarine Cladophora in culture', Bot. Mar. 24, 93–106.Google Scholar
  31. Gordon, D. M., van den Hoek, C. and McComb, A. J.: 1985, 'An aegagropiloid form of the green alga Cladophora montagneana Kütz. (Chlorophyta, Cladophorales) from Southwestern Australia', Bot. Mar. 27, 57–65.Google Scholar
  32. Grime, J. P.: 1974, 'Vegetation classification by reference to strategies', Nature 250, 26–31.Google Scholar
  33. Grime, J. P.: 1979, Plant Strategies and Vegetation Processes, John Wiley & Sons, Chichester.Google Scholar
  34. Haines, K. C. and Wheeler, P. A.: 1978, 'Ammonium and nitrate uptake rates of the seaweeds Hypnea musciformis (Rhodophyta) and Macrocystis pyrifera (Phaeophyta)', J. Phycol. 14, 319–324.Google Scholar
  35. Hanisak, M. D.: 1983, 'The nitrogen relationships of marine macroalgae', in E. J. Carpenter and D. G. Capone (eds.), Nitrogen in the Marine Environment, Academic Press, N.Y, pp. 699–730.Google Scholar
  36. Harlin, M. M. and Craigie, J. S.: 1978, 'Nitrate uptake by Laminaria longicuris (Phaeophyceae)', J. Phycol. 14, 464–467.Google Scholar
  37. Harlin, M. M.: 1978, 'Nitrate uptake by Enteromorpha spp. (Chlorophyceae): Applications to aquaculture systems', Aquaculture 15, 373–376.Google Scholar
  38. Harrison, P. J. and Druehl, L. D.: 1982, 'Nutrient uptake and growth in the Laminanales and other macrophytes: A consideration of methods', in L. M. Srivastava (ed.), Synthetic and Degradative Processes in Marine Macrophytes, Waller de Gruyter, Berlin, pp. 99–120.Google Scholar
  39. Harrison, P. J., Parslow, J. S. and Conway, H. L.: 1989, 'Determination of nutrient uptake kinetic parameters: a comparison of methods', Mar. Ecol. Prog. Ser. 52, 301–312.Google Scholar
  40. Healey, F. P.: 1980, 'Slope of the Monod equation as an indicator of advantage in nutrient competition', Microbial Ecol. 5, 281–286.Google Scholar
  41. Henley, W. J. and Ramus, J.: 1989, 'Time course of physiological response to Ulva rotundata to growth irradiance transitions', Mar. Ecol. Prog. Ser. 54, 171–177.Google Scholar
  42. Hiscock, K.: 1981, 'South west Britain sublittoral survey - final report', CSD Report No. 327, Report from Oil Pollution Research Unit, Field Studies Council to Nature Conservancy Council.Google Scholar
  43. Innes, D. J.: 1988, 'Genetic differentiation in the intertidal zone in populations of the alga Enteromorpha linza (Ulvales: Chlorophyta)', Mar. Biol. 97, 9–16.Google Scholar
  44. Innes, S. and Louigne, D. M.: 1989, 'Size of aquatic endotherms', Nature 341, 192.Google Scholar
  45. Kamermans, P., Malta, E-J., Verschuure, J. M., Lentz, L. F. and Schrijvers, L.: 1998, 'Role of cold resistance and burial for winter survival and spring initiation of an Ulva spp. (Chlorophyta) bloom in a eutrophic lagoon (Veerse Meer lagoon, the Netherlands)', Mar. Biol. 131, 45–51.Google Scholar
  46. Karsten, U., Wiencke, C. and Kirst, G. O.: 1990, 'The beta-dimethylsulphoniopropionate (DMSP) content of macroalgae from Antarctica and Southern Chile', Bot. Mar. 33, 143–146.Google Scholar
  47. Kautsky, L.: 1982, 'Primary production and uptake kinetics of ammonium and phosphate by Enteromorpha compressa in an ammonium sulphate industry outlet area', Aquat. Bot. 12, 23–40.Google Scholar
  48. Kim, K. Y. and Lee, I. K.: 1996, 'The germling growth of Enteromorpha intestinalis (Chlorophyta) in laboratory culture under different combinations of irradiance and salinity and temperature and salinity', Phycologia 35, 327–331.Google Scholar
  49. Kim, K. Y., Kyu-Lee, I. and Chung, I. C.: 1990, 'Effects of temperature and salinity on germination and vegetative growth of Enteromorpha multiramosa Bliding (Chlorophyceae, Ulvales)', Korean J. Bot. 33, 141–146.Google Scholar
  50. Kindig, A. C. and Littler, M. M.: 1980, 'Growth and primary productivity of marine macrophytes exposed to domestic sewage effluents', Mar. Environ. Res. 3, 81–100.Google Scholar
  51. Lapointe, B. E. and Tenore, K. R.: 1981, 'Experimental outdoor studies with Ulva fasciata Delile. Interaction of light and nitrogen on nutrient uptake, growth and biochemical composition', J. Exp. Mar. Biol. Ecol. 53, 135–152.Google Scholar
  52. Lavery, P. S. and McComb, A. J.: 1991, 'Macroalgal-sediment nutrient interactions and their importance to macroalgal nutrition in a eutrophic estuary', Estuar. Coast. Shelf Sci. 32, 281–295.Google Scholar
  53. Little, C. and Smith, L. P.: 1980, 'Vertical zonation on rocky shores in the Severn Estuary, U.K.', Estuarine Coastal Mar. Sci. 11, 651–670.Google Scholar
  54. Littler, M. M. and Littler, D. S.: 1980, 'The evolution of thallus form and survival strategies in benthic marina macroalgae: Field and laboratory tests of a functional form model', Am. Nat. 116, 25–44.Google Scholar
  55. MacGarvin, M.: 1995, 'Marine eutrophication in the U.K.: A discussion document', Report to the World Wide Fund for Nature U.K., 23 pp.Google Scholar
  56. McComb, A. J., Atkins, R. P., Birch, P. B., Gordon D. M. and Lukatelich R. J.: 1981, 'Eutrophication in the Peel-Harvey Estuarine System,Western Australia', in B. J. Neilson and L. E. Cronin (eds.), Estuaries and Nutrients, Humana Press, New Jersey, pp. 323–342.Google Scholar
  57. Montgomery, H. A. and Soulsby, P. G.: 1980, 'Effects of eutrophication on the intertidal ecology of Langstone Harbour, U.K., and proposed control measures', Prog. Water Technol. 13, 287–294.Google Scholar
  58. Morand, P. and Briand, X.: 1996, 'Excessive growth of macroalgae: A symptom of environmental disturbance', Bot. Mar. 39, 491–516.Google Scholar
  59. Moss, B.: 1995, 'The microwaterscope - A four-dimensional view of interactions among water chemistry, phytoplankton, periphyton, macrophytes, animals and ourselves', Water Sci. Technol. 32, 105–116.Google Scholar
  60. Moss, B.: 1999, 'From algal culture to ecosystem: From information to culture', Eur. J. Phycol. 34, 193–203.Google Scholar
  61. Neilsen, S. L. and Sand-Jensen, K.: 1990, 'Allometric scaling of maximal photosynthetic growth rate to surface-volume ratio', Limnol. Oceanogr. 35, 177–181.Google Scholar
  62. Nicholls, D. J., Tubbs, C. R. and Haynes, F. N.: 1981, 'The effect of green algal mats on intertidal macrobenthic communities and their predators', Kiel. Meeresforsch. Sonderh. 5, 511–520.Google Scholar
  63. Nienhuis, P. H.: 1992, 'Ecology of coastal lagoons in the Netherlands (Veerse Meer and Grevelingen)', Vie Milieu, 42, 59–72.Google Scholar
  64. O'Brien, M. C. and Wheeler, P. A.: 1987, 'Short term uptake of nutrients by Enteromorpha prolifera (Chlorophyceae)', J. Phycol. 23, 547–556.Google Scholar
  65. Odum, E. P., Kuenzler, E. J. and Blint, M. X.: 1958, 'Uptake of P32 and primary productivity in marine benthic algae', Limnol. Oceanogr. 3, 340–345.Google Scholar
  66. Parr, W. and Norton, R. L.: 1994, 'Eutrophication of tidal waters: Classification and screening tools', WRc Report No. SR 3707.Google Scholar
  67. Parr, W.: 1994, 'Eutrophication of the Wash: Factors and interactions', WRc Report No. CO 3752.Google Scholar
  68. Pedersen, M. F. and Borum, J.: 1997, 'Nutrient control of estuarine macroalgae: Growth strategy and the balance between nitrogen requirements and uptake', Mar. Ecol. Prog. Ser. 161, 155–163.Google Scholar
  69. Pedersen, M. F.: 1994a, 'Voekst of neeringsdynamik los marine planter', Ph.D. Thesis, University of Copenhagen.Google Scholar
  70. Pedersen, M. F.: 1994b, 'Transient ammonium uptake in the macroalga Ulva lactuca (Chlorophyta) - Nature, regulation and the consequences for choice of measuring technique', J. Phycol. 30, 980–986.Google Scholar
  71. Phillips, G. L., Eminson, D. F. and Moss, B.: 1978, 'A mechanism to account for macrophyte decline in progressively eutrophicated waters', Aquat. Bot. 4, 103–126.Google Scholar
  72. Poole, L. J. and Raven, J. A.: 1997, 'The biology of Enteromorpha', in F. E. Round and D. J. Chapman (eds.), Progress in Phycological Research, Vol. 13, Biopress, Bristol, pp. 1–148.Google Scholar
  73. Post, A. and Larkum, A. W. D.: 1993, 'UV-absorbing pigments, photosynthesis and UV exposure in Antarctica: Comparison of terrestrial and marine algae', Aquat. Bot. 45, 231–243.Google Scholar
  74. Probyn, T. A.: 1984, 'Nitrate uptake by Chordaria flagelliformis (Phaeophyta)', Bot. Mar. 17, 271–275.Google Scholar
  75. Raffaelli, D., Raven, J. A. and Poole, L. J.: 1998, 'Ecological impact of mass blooms of benthic algae', Mar. Biol. Oceanogr. Ann. Rev. 36, 97–25.Google Scholar
  76. Raffaelli, D. G., Balls, P., Way, S., Patterson, I. J., Hohmann, S. and Corp, N.: 1999, 'Major long term changes in the ecology of the Ythan estuary, Aberdeenshire, Scotland: How important are physical factors?', Aquat. Cons. 9, 219–236.Google Scholar
  77. Raffaelli, D. G., Hull, S. and Milne, H.: 1989, 'Long-term changes in nutrients, weed mats and shorebirds in an estuarine system', Cah. Bio. Mar. 30, 259–270.Google Scholar
  78. Raffaelli, D. G., Limia, J., Hull, S. and Pont, S.: 1991, 'Interactions between invertebrates and macroalgal mats on estuarine mudflats', J. Mar. Biol. Assoc. (U.K.) 71, 899–908.Google Scholar
  79. Raven, J. A. and Edwards, D.: 2001, 'Roots: Evolutionary origins and biogeochemical significance', J. Exp. Bot. 52, 381–401.Google Scholar
  80. Raven, J. A. and Johnston, A. M.: 1991, 'Photosynthetic carbon assimilation by Prasiola stipitata (Prasiolales, Chlorophyta) under emersed and submersed conditions: Relationship to the taxonomy of Prasiola', Br. Phycol. J. 26, 247–257.Google Scholar
  81. Raven, J. A. and Yin, Z-H.: 1998, 'The past, present and future of nitrogenous compounds in the atmosphere and their interactions with plants', New Phytol. 139, 205–219.Google Scholar
  82. Raven, J. A.: 1984, Energetics and Transport in Aquatic Plants, Alan R. Liss, New York.Google Scholar
  83. Raven, J. A.: 1997, 'The role of marine biota in the evolution of terrestrial biota: Gases and genes', Biogeochem. 39, 139–164.Google Scholar
  84. Raymont, J. E. G.: 1980, Phytoplankton and Productivity in the Oceans, 2nd ed. Vol. 1. Phytoplankton, Pergamon Press, Oxford, 489 pp.Google Scholar
  85. Rindi, F., Guiry, M. D., Barbier, R. P. and Cinelli, F.: 1999, 'The marine and terrestrial Prasiolales (Chlorophyta) of Galway City, Ireland: A morphological and ecological study', J. Phycol. 35, 469–482.Google Scholar
  86. Rosemarin, A. S.: 1982, 'Phosphorus nutrition of two potentially competing filamentous algae, Cladophora glomerata (L.) Kütz and Stigeoclonium tenue (Agardh) Kütz from Lake Ontario', J. Great Lakes Res. 8, 66–72.Google Scholar
  87. Rosenberg, G. and Ramus, J.: 1984, 'Uptake of inorganic nitrogen and seaweed surface area: Volume ratios', Aquat. Bot. 19, 65–72.Google Scholar
  88. Rosenberg, G.: 1981, 'Ecological growth strategies in the seaweeds Gracilaria foliifera (Rhodophyceae) and Ulva sp. (Chlorophyceae)', Ph.D. Thesis, Yale University, New Haven, Connecticut, 151 pp.Google Scholar
  89. Round, F. E.: 1981, The Ecology of Algae, Cambridge University Press, Cambridge.Google Scholar
  90. Sand-Jensen, K.: 1988, 'Photosynthetic responses of Ulva lactuca at very low light', Mar. Ecol. Prog. Ser. 50, 195–201.Google Scholar
  91. Scheffer, M., Mospen, S. H., Meijer, M. L., Moss, B. and Jeppesen, E.: 1993, 'Alternative equilibria in shallow lakes', Trends Ecol. Evoln. 8, 275–279.Google Scholar
  92. Schories, D.: 1995, 'Sporulation of Enteromorpha spp. (Chlorophyta) and overwintering of spores in sediments of the Wadden Sea, Island of Sylt, North Sea', Neth. J. Aquat. Ecol. 29, 341–347.Google Scholar
  93. Schramm, W.: 1996, 'The Baltic sea and its transition zones', in W. Schramm and P. Neinhuis (eds.), Ecological Studies, Vol. 123. Marine Benthic Vegetation: Recent Changes and the Effects of Eutrophication, Springer-Verlag, Berlin, pp. 131–164.Google Scholar
  94. Sfriso, A., Marcomini, A. and Pavoni, B.: 1987, 'Relationships between macroalgal biomass and nutrient concentrations in a hypertrophic area of the Venice Lagoon', Mar. Environ. Res. 22, 297–312.Google Scholar
  95. Sfriso, A., Raccanelli, S., Pavoni, B. and Marcomini, A.: 1991, 'Sampling strategies for measuring macroalgal biomass in the shallow waters of the Venice Lagoon', Environ. Technol. Lett. 6, 24–29.Google Scholar
  96. Shellem, B. H. and Josselyn, M. N.: 1982, 'Physiological ecology of Enteromorpha clathrata (Roth) Grev. on a salt marsh mudflat', Bot. Mar. 25, 541–549.Google Scholar
  97. Smith, R. E. H. and Kalf, J.: 1982, 'Size dependent phosphorus uptake kinetics and cell quota in phytoplankton', J. Phycol. 18, 275–284.Google Scholar
  98. Southwood, T. R. E.: 1977, 'Habitat, the template for ecological strategies?', J. Animal Ecol. 46, 337–365.Google Scholar
  99. Tan, I. H., Blomster J., Hansen, G., Leskinen, E., Maggs, C. A., Mann, D. G., Sluiman, H. J. and Stanhope, M. J.: 1999, 'Molecular phylogenetic evidence for a reversible morphogenetic switch controlling the gross morphology of two common genera of green seaweeds, Ulva and Enteromorpha', Mol. Biol. Evoln. 16, 1011–1018.Google Scholar
  100. Taylor, R. and Raven, J. A.: 2002, 'Survival strategies of Enteromorpha from eutrophic sites', Coastal Zone Topics Series (in press).Google Scholar
  101. Taylor, R., Fletcher, R. L. and Pye, K.: 1998, 'The “green tide” phenomenon in the North Sea and English Channel: Case studies of the Ythan estuary and Langstone Harbour', in G.W. Scott and I. Tittley (eds.), Changes in the Marine Flora of the North Sea, CERCI Publications, Scarborough, 166 pp.Google Scholar
  102. Taylor, R., Fletcher, R. L. and Raven, J. A.: 2001, 'The growth of selected “green tide” algae in laboratory culture - effects of irradiance, temperature, salinity and nutrients on growth rate', Bot. Mar. 44, 327–336.Google Scholar
  103. Taylor, R.: 1997, 'The ecophysiology of “green tide” algae from Langstone Harbour, south coast of England', Ph.D. Thesis, University of Portsmouth.Google Scholar
  104. Taylor, R.: 1999, 'The “green tide” threat in the U.K. - A brief overview with particular reference to Langstone Harbour, south coast of England and the Ythan Estuary, east coast of Scotland', Bot. J. Scotland 51, 195–203.Google Scholar
  105. Thomas, T.E, Harrison, P. J. and Taylor, E. B.: 1985, 'Nitrogen uptake and growth of the germlings and mature thalli of Fucus distichus', Mar. Biol. 84, 267–274.Google Scholar
  106. Thomas, T. E. and Harrison, P. J.: 1987, 'Rapid ammonium uptake and nitrogen interactions in five intertidal seaweeds grown under field conditions', J. Exp. Mar. Biol. Ecol. 107, 1–8.Google Scholar
  107. Tompsett, P. E.: 1994, 'Helford river survey. Monitoring Report No. 4 for 1993', Report to World Wide Fund for Nature U.K.. Topinka, J. A.: 1978, 'Nitrogen uptake by Fucus spiralis (Phaeophyceae)', J. Phycol. 14, 241–247.Google Scholar
  108. Van Tuinen, M., Butvill, D. B., Kirsch, J. A. W. and Hedges, S. B.: 2001, 'Convergence and divergence in the evolution of aquatic birds', Proc. R. Soc. Lond. B 268, 1345–1350.Google Scholar
  109. Vermaat, J. E. and Sand-Jensen, K.: 1987, 'Survival, metabolism and growth of Ulva lactuca under winter conditions: A laboratory study of bottlenecks in the life cycle', Mar. Biol. 95, 55–61.Google Scholar
  110. Wallentinus, I.: 1984, 'Comparisons of nutrient uptake rates for Baltic macroalgae with different thallus morphologies', Mar. Biol. 80, 215–225.Google Scholar
  111. Wallentinus, I.: 1991, 'The Baltic Sea gradient', in A. C. Mathieson and P. H. Nienhuis (eds.), Ecosystems of the World - 24 Intertidal and littoral ecosystems, Elsevier, Amsterdam, pp. 83–108.Google Scholar
  112. Warwick, R. M., Davey, J. T., Gee, J. M. and George, C. L.: 1982, 'Faunistic control of Enteromorpha blooms: A field experiment', J. Exper. Marine Biol. & Ecol. 56, 23–31.Google Scholar
  113. Wheeler, W. N. and Neushul, M.: 1981, 'The aquatic environment', in O. L. Lange, P. S. Nobel, C. B. Osmond and H. Ziegler (eds.), Encyclopedia of Plant Physiology. Vol. 12A: Physiological Plant Ecology. I. Responses to the Physical Environment, Springer-Verlag, Berlin, pp. 229–247.Google Scholar
  114. Young, A. J., Collins, J. C. and Russell, G.: 1987, 'Solute regulation in the euryhaline marine alga Enteromorpha prolifera (O.F. Mull)', J. Ag. J. Exp. Bot. 38, 1298–1308.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  1. 1.Division of Environmental and Applied Biology, School of Life SciencesUniversity of DundeeDundeeU.K. (Author for correspondence

Personalised recommendations