Abstract
The seasonal variation in growth rate of a population of Laminaria digitata (Huds.) Lamour growing at Arbroath, Scotland was studied between August 1981 and September 1982, and was found to follow the biphasic annual cycle typical of this genus. Growth rates were maximum (0.3 cm cm-1 mo-1) in early June and minimum (0.05 cm cm-1 mo-1) between September and January. An analysis of the relationship between the seasonal changes in environmental factors (inorganic nitrogen concentrations, irradiance and temperature) with those of growth rate and the accumulation or mobilisation of cellular reserves of carbohydrates and nitrate, indicated that growth was nitrogen-limited between June and October and light-limited (with a possible co-involvement of temperature) for the remainder of the year. These conclusions were supported by the seasonal changes in the ratio of actual: potential in-vivo nitrate reductase activities in L. digitata, thus confirming the suitability of this technique for monitoring the occurrence of nitrogen limitation in Laminaria spp. The seasonal changes in blade nitrate reductase activities closely followed those of growth rate, with maximum activities [0.3 μmol NO -3 reduced g-1 (wet wt) h-1] being present in late May and minimum levels [0.01 μmol NO -3 reduced g-1 (wet wt) h-1] occurring between November and March. The correlation observed between nitrate reductase activities and growth rate is consistent with the ability of Laminaria spp. to store excess inorganic nitrogen, available during winter and early spring, as NO -3 , and with the requirement to conserve enzyme protein during the summer period of nitrogen limitation.
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Literature cited
Anderson, M. R., A. Cardinal and J. Larochelle: An alternative growth pattern for Laminaria longicruris. J. Phycol. 17, 405–411 (1981)
Beevers, L. and R. H. Hageman: Nitrate reduction in higher plants. A. Rev. Plant Physiol. 20, 495–522 (1969)
Black, W. A. P.: The seasonal variation in chemical constitution of some of the sublittoral seaweeds common to Scotland. Part 1. Laminaria cloustoni. J. Soc. chem. Ind., Lond. 67, 165–176 (1948)
Black, W. A. P.: The seasonal variation in weight and chemical composition of the common British Laminariaceae. J. mar. biol. Ass. U.K. 29, 45–72 (1950)
Black, W. A. P. and E. T. Dewar: Correlation of some of the physical and chemical properties of the sea with the chemical constitution of the algae. J. mar. biol. Ass. U.K. 28, 673–699 (1949)
Bolton, J. J. and K. Lüning: Optimal growth and maximal survival temperatures of Atlantic Laminaria species (Phaeophyta) in culture. Mar. Bot. 66, 89–94 (1982)
Buggeln, R. G.: Physiological investigations on Alaria esculenta (Laminariales, Phaeophyceae). II. Role of translocation in blade growth. J. Phycol. 13, 212–218 (1977)
Buggeln, R. G.: Physiological investigations on Alaria esculenta (Laminariales, Phaeophyceae). IV. Inorganic and organic nitrogen in the blade. J. Phyciol. 14, 156–160 (1978)
Calvin, N. I. and R. J. Ellis: Growth of subtidal Laminaria groenlandica in southeastern Alaska related to season and depth. Bot. mar. 24, 107–114 (1981)
Chapman, A. R. O. and J. S. Craigie: Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar. Biol. 40, 197–205 (1977)
Chapman, A. R. O. and J. E. Lindley: Seasonal growth of Laminaria solidungula in the Canadian high Arctic in relation to irradiance and dissolved nutrient concentrations. Mar. Biol. 57, 1–5 (1980)
Chapman, A. R. O., J. W. Markham and K. Lüning: Effects of nitrate concentration on the growth and physiology of Laminaria saccharina (Phaeophyta) in culture. J. Phycol. 14, 195–198 (1978)
Cosson, J.: Etude d'une population de Laminaria digitata, Lam. (Biométrie, Croissance, Régénération). Bull. Soc. Linn. Normandie 8, 268–281 (1967)
Davison, I. R.: Nitrogen metabolism of Laminaria digitata (Huds.) Lamour, 199 pp. Ph.D. thesis University of Dundee 1983
Davison, I. R. and R. H. Reed. Osmotic adjustment in Laminaria digitata (Phaeophyta) with particular reference to seasonal changes in internal solute concentrations. J. Phycol. 21, 1985
Davison, I. R. and W. D. P. Stewart: Occurrence and significance of nitrogen transport in the brown alga Laminaria digitata. Mar. Biol. 77, 107–112 (1983)
Davison, I. R. and W. D. P. stewart: Studies on nitrate reductase activity in Laminaria digitata (Huds.) Lamour. I. Longitudinal and transverse profiles of nitrate reductase activity within the thallus. J. exp. mar. Biol. Ecol. 74, 201–210 (1984a)
Davison, I. R. and W. D. P. Stewart: Studies on nitrate reductase activity in Laminaria digitata (Huds.) Lamour. II. The role of nitrate availability in the regulation of enzyme activity. J. exp. mar. Biol. Ecol. 79, 65–78 (1984b)
DeBoer, J. A.: Nutrients. In: The biology of seaweeds, pp 356–392. Ed. by C. S. Lobban and M. J. Wynne. London: Blackwell Scientific Publications 1981
Dieckmann, G. S.: Aspects of the ecology of Laminaria pallida (Grev.) J. Ag. off the Cape Penninsula (South Africa). I. Seasonal growth. Bot. mar. 23, 579–585 (1980)
Espinoza, J. and A. R. O. Chapman: Ecotypic differentiation of Laminaria longicruris in relation to seawater nitrate concentration. Mar. Biol. 74, 213–218 (1983)
Evans, G. C.: The quantitative analysis of plant growth, 734 pp. Oxford: Blackwell Publishing Company 1972
Fortes, M. D. and K. Lüning: Growth rates of North Sea macroalgae in relation to temperature, irradiance and photoperiod. Helgoländer wiss. Meeresunters. 34, 15–29 (1980)
Gagné, J. A., K. H. Mann and A. R. O. Chapman: Seasonal patterns of growth and storage in Laminaria longicruris in relation to differing patterns of availability of nitrogen in the water. Mar. Biol. 69, 91–101 (1982)
Gerard, V. A. and K. H. Mann: Growth and production of Laminaria longicruris (Phaeophyta) populations exposed to different intensities of water movement. J. Phycol. 15, 33–41 (1979)
Gillbricht, M.: Hydrographie, Nährstoffe und Phytoplankton bei Helgoland. In: Biologische Anstalt Helgoland, Jahresbericht 1982, pp 23–27. Ed. by H. Westernhagen. Heide: Westholsteinische Verlagsdruckerei Boysens and Co. 1982
Harlin, M. M. and J. S. Craigie: Nitrate uptake by Laminaria longicruris (Phaeophyceae). J. Phycol. 14, 464–467 (1978)
Harrison, P. J. and L. D. Druehl: Nutrient uptake and growth in the Laminariales and other macrophytes: a consideration of methods. In: Synthetic and degradative processes in marine macrophytes, pp 99–120. Ed. by L. M. Srivastava. Berlin: Walter de Gruyter and Company 1982
Holligan, P. M. and E. A. Drew: Routine analysis by gas-liquid chromatography of soluble carbohydrates in extracts of plant tissues. II. Quantitative analysis of standard carbohydrates, and the separation and estimation of soluble sugars and polyols from a variety of plant tissues. New Phytol. 70, 271–297 (1971)
Kain, J. M.: Synopsis of biological data on Laminaria hyperborea, 65 pp. Rome: F.A.O. Fisheries Synopsis No.87 1971
Kain, J. M.: A view of the genus Laminaria. Oceanogr. mar. Biol. A. Rev. 17, 101–161 (1979)
Küppers, U. and M. Weidner: Seasonal variation of enzyme activities in Laminaria hyperborea. Planta 148, 222–230 (1980)
Larsen, B. and A. Jensen: The determination of nitrate and nitrite in algal material, and the seasonal variations in the nitrate content of some Norwegian seaweeds, 22 pp. Oslo: Norwegian Institute of Seaweed Research 15, 1957
Lewis, J. R.: The ecology of rocky shores, 323 pp. London: Hodder and Stoughton 1964
Lüning, K.: Growth strategies of three Laminaria species (Phaeophyceae) inhabiting diffeent depth zones in the sublittoral region of Helgoland (North Sea). Mar. Ecol. Prog. Ser. 1, 195–207 (1979)
Lüning, K.: Seasonality in larger brown algae and its possible regulation by the environment. In: Synthetic and degradative processess in marine macrophytes, pp 47–65. Ed. by L. M. Srivastava. Berlin: Walter de Gruyter and Company 1982
Lüning, K.: Photoperiodism in Laminaria hyperborea. Helgoländer Meeresunters. (1984)
Lüning, K. and M. J. Dring: Continuous underwater light measurement near Helgoland (North Sea) and its significance for characteristic light limits in the sublittoral region. Helgoländer wiss. Meeresunters. 32, 403–424 (1979)
Lüning, K., K. Schmitz and J. Willenbrink: CO2 fixation and translocation in Benthic marine algae. III. Rates and ecological significance of translocation in Laminaria hyperborea and L. saccharina. Mar. Biol. 23, 275–281 (1973)
Mackereth, F. J. H., J. Heron and J. F. Talling: Water analysis. F.B.A. Publication No. 36, 120 pp. Kendall: Freshwater Biological Association 1978
Manley, S. L.: Composition of sieve tube sap from Macrocystis pyrifera (Phaeophyceae) with emphasis on the inorganic constituents. J. Phyciol. 19, 118–121 (1983)
Mann, K. H.: Ecological energetics of the sea-weed zone in a marine bay on the Atlantic coast of Canada. II. Productivity of the seaweeds. Mar. Biol. 14, 199–209 (1972)
Parke, M.: Studies on British Laminariaceae. I. Growth in Laminaria saccharina (L.) Lamour. J. mar. biol. Ass. U.K. 27, 651–709 (1948)
Pérez, R.: Ecologie, croissance et regeneration teneurs en acide alginique de Laminaria digitata sur les Cotes Francaises de la Manche. Rev. Trav. Inst. Peches marit. 35, 287–346 (1971)
Probyn, T. A. and A. R. O. Chapman: Summer growth of Chordaria flagelliformis (O. F. Muell.) C. Ag.: physiological strategies in a nutrient stressed environment. J. exp. mar. Biol. Ecol. 73, 243–271 (1983)
Reed, R. H., I. R. Davison, J. A. Chudek and R. Foster: The osmotic role of mannitol in the Phaeophyta: an appraisal. Phytochemistry (In press)
Schmitz, K.: Translocation. In: The biology of seaweeds, pp 534–558. Ed. by C. S. Lobban and M. J. Wynne. London: Blackwell Scientific Publications 1981
Schmitz, K., K. Lüning and J. Willenbrink: CO2 Fixierung und Stofftransport in benthischen marinen Algen. II. Zum Ferntransport 14C-markierter Assimilate bei Laminaria hyperborea und Laminaria saccharina. Z. Pflanzenphysiol. 67, 418–429 (1972)
Schmitz, K. and L. M. Srivastava: On the fine structure of sieve tubes and the physiology of assimilate transport in Alaria marginata. Can. J. Bot. 53, 861–876 (1975)
Strickland, J. D. H. and T. R. Parsons: A practical handbook of seawater analysis, 2nd ed. Bull. Fish. Res. Bd Can. 167, 1–311 (1972)
Sundene, O.: On the ecology of Laminaria digitata in Norway in view of transplant experiments. Nytt. Mag. Bot. 11, 83–107 (1964)
Wheeler, W. N. and M. Weidner: Effects of external inorganic nitrogen concentration on metabolism, growth and activities of key carbon and nitrogen assimilatory enzymes of Laminaria saccharina (Phaeophyceae) in culture. J. Phycol. 19, 92–96 (1983)
Yamaguchi, T., T. Ikawa and K. Nisizawa: Pathway of mannitol formation during photosynthesis in brown algae. Plant Cell Physiol. 10, 425–440 (1969)
Yemm, E. W. and A. J. Willis: The estimation of carbohydrates in plant extracts by Anthrone. Biochem. J. 57, 508–514 (1954)
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Davison, I.R., Andrews, M. & Stewart, W.D.P. Regulation of growth in Laminaria digitata: use of in-vivo nitrate reductase activities as an indicator of nitrogen limitation in field populations of Laminaria spp.. Mar. Biol. 84, 207–217 (1984). https://doi.org/10.1007/BF00393006
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DOI: https://doi.org/10.1007/BF00393006