Abstract
Ulva curvata (Kutz.) de Toni growing in shallow estuaries experiences a highly variable supply of dissolved inorganic N, which can limit growth rates. The effects of N supply variability and annual temperature and light variation on growth rates and chemical composition were assessed in plants grown in outdoor tanks supplied with running seawater and either pulsed or continuous N additions for 8 d. Environmental variables were measured every 12 h, growth rates every 2 d, and plant nitrogenous constituents every 4 d. The experiment was repeated 7 times over the course of a year. The slopes of growth rate-tissue N and growth rate-N supply plots increased with temperature and varied at periods at least as short as 2 d. Temperature explained 44% of variation in growth rate, and temperature, light, and N supply together explained 53% of variation in growth rate. N-limitation occurred only above 20°C, the approximate temperature for the maximum growth rate. Growth rate and tissue N were not affected by N supply frequency. Tissue N, ribulose-bisphosphate carboxylase activity, and chlorophyll contents were correlated with each other and with environmental variables but not with growth rate. U. curvata thus does not maintain balanced growth in the strict sense, but rather stores nutrients supplied as pulses for use when they become growth-limiting. Since the relative importance of any single growth-limiting factor is highly dynamic, assessing the importance of multiple limiting factors requires longterm, high-frequency sampling of principal limiting factors and seaweed growth rates.
Similar content being viewed by others
Literature cited
Allen, T. F. H. (1977) Scale in microscopic algal ecology: a neglected dimension. Phycologia 16: 253–257
Chapman, A. R. O., Craigie, J. S. (1977). Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar. Biol. 40: 197–205
Cotton, A. D. (1910). On the growth of Ulva latissima L. in water polluted by sewage. Kew Bull. 191: 15–19
Davison, I. R., Andrews, M., Stewart, W. D. P. (1984). 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
Dean, T. A., Jacobsen, F. R. (1984). Growth of juvenile Macrocystis pyrifera (Laminariales) in relation to environmental factors. Mar. Biol. 83: 301–311
DeBoer, J. A., Guigli, H. J., Israel, T. L., D'Elia, C. F. (1978). Nutritional studies of two red algae. I. Growth rate as a function of nitrogen source and concentration. J. Phycol. 14: 261–266
D'Elia, C. F., DeBoer, J. A. (1978). Nutritional studies of two red algae. II. Kinetics of ammonium and nitrate uptake. J. Phycol. 14: 266–272
Duke, C. S. (1985). Temporal scales of nitrogen availability and seaweed physiological response. Ph. D. thesis, Duke University, Durham, North Carolina
Duke, C. S., Lapointe, B. E., Ramus, J. (1986) Effects of light on growth, RuBPCase activity, and chemical composition of Ulva species (Chlorophyta). J. Phycol. 22: 362–370
Duke, C. S., Litaker, R. W., Ramus, J. (1987). Seasonal variation in RuBPCase activity and N allocation in the chlorophyte seaweeds Ulva curvata (Kutz.) De Toni and Codium decorticatum (Woodw.) Howe. J. exp. mar. Biol. Ecol. 112: 145–164
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
Haines, K. C., Wheeler, P. A. (1977). Ammonia and nitrate uptake rates of the seaweeds Hypnea musciformis (Rhodophyta) and Macrocystis pyrifera (Phaeophyta). J. Phycol. 13 (suppl.): 26
Hanisak, M. D., Harlin, M. M. (1978). Uptake of inorganic nitrogen by Codium fragile subsp. tomentosoides (Chlorophyta). J. Phycol. 14: 450–454
Hanks, R. W. (1966). Observations on “milky water” in Chesapeake Bay. Ches. Sci. 7: 175–176
Harris, G. P. (1980). Temporal and spatial scales in phytoplankton ecology. Mechanisms, methods, models, and management. Can. J. Fish. Aquat. Sci. 37: 877–900
Jeffrey, S. W., Humphrey, G. F. (1975). New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae, and natural phytoplankton. Biochem. Physiol. Pfl. 167: 191–194
Koroleff, F. (1970). Direct determination of ammonia in natural waters as indophenol blue. ICES. Information on techniques and methods for seawater analysis. Interlab. No. 3: 19–22
Lapointe, B. E. (1985). Strategies for pulsed nutrient supply to Gracilaria cultures in the Florida Keys: interactions between concentration and frequency of nutrient pulses. J. exp. mar. Biol. Ecol. 93: 211–222
Lapointe, B. E., Dawes, C. J., Tenore, K. R. (1984). Interactions between light and temperature on the physiological ecology of Gracilaria tikvahiae (Gigartinales: Rhodophyta). II. Nitrate uptake and levels of pigments and chemical constituents. Mar. Biol. 80: 171–178
Lapointe, B. E., Duke, C. S. (1984). Biochemical strategies for growth of Gracilaria tikvahiae (Rhodophyta) in relation to light intensity and nitrogen availability. J. Phycol. 20: 488–495
Lapointe, B. E., Tenore, K. R. (1981). Experimental outdoor studies with Ulva fasciata Delile. I. Interaction of light and nitrogen on nutrient uptake, growth and biochemical composition. J. exp. mar. Biol. Ecol. 53: 135–152
Laws, E. A., Bannister, T. T. (1980). Nutrient-and light-limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean. Limnol. Oceanogr. 25: 457–473
Litaker, R. W., Duke, C. S., Kenney, B. E., Ramus, J. (1987). Short-term environmental variability and phytoplankton abundances in a shallow tidal estuary. I. Winter and summer. Mar. Biol. 96: 115–121
Perry, M. J., Talbot, M. C., Alberte, R. S. (1981). Photoadaptation in marine phytoplankton: response of the photosynthetic unit. Mar. Biol. 62: 91–101
Probyn, T. A., Chapman, A. R. O. (1983). 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
Rhee, G.-Y., Gotham, I. J. (1981a). The effect of environmental factors on phytoplankton growth: Temperature and the interactions of temperature with nutrient limitation. Limnol. Oceangr. 26: 635–648
Rhee, G.-Y., Gotham, I. J. (1981b). The effect of environmental factors on phytoplankton growth: Light and the interactions of light with nitrate limitation. Limnol. Oceangr. 26: 649–659
Rosenberg, G. (1981). Ecological growth strategies in the seaweeds Gracilaria foliifera (Rhodophyceae) and Ulva sp. (Chlorophyceae). Ph. D. thesis, Yale University, New Haven, Connecticut
Rosenberg, G., Paerl, H. W. (1981). Nitrogen fixation by blue-green algae associated with the siphonous green seaweed Codium decorticatum: effects on ammonium uptake. Mar. Biol. 61: 151–158
Rosenberg, G., Probyn, T. A., Mann, K. H. (1984). Nutrient uptake and growth kinetics in brown seaweeds: response to continuous and single additions of ammonium. J. exp. mar. Biol Ecol. 80: 125–146
Rosenberg, G., Ramus, J. (1981). Ecological growth strategies in the seaweeds Gracilaria foliifera (Rhodophyceae) and Ulva sp. (Chlorophyceae): The rate and timing of growth. Bot. mar. 24: 583–589
Rosenberg, G., Ramus, J. (1982). Ecological growth strategies in the seaweeds Gracilaria foliifera (Rhodophyceae) and Ulva sp. (Chlorophyceae): Soluble nitrogen and reserve carbohydrates. Mar. Biol. 66: 251–259
Seeman, J. R., Sharkey, T. D., Wang, J. L., Osmond, C. B. (1987). Environmental effects on photosynthesis, nitrogen-use efficiency, and metabolite pools in leaves of sun and shade plants. Plant Physiol. 84: 796–802
Shivji, M. S. (1985). Interactive effects of light and nitrogen on growth and chemical composition of juvenile Macrocystis pyrifera (L.) C. Ag. (Phaeophyta) sporophytes. J. exp. mar. Biol. Ecol. 89: 81–96
Sokal, R. R., Rohlf, F. J. (1981). Biometry. W. H. Freeman and Co., San Francisco
Stanier, R. Y., Ingraham, J. L., Wheelis, M. L., Painter, P. R. (1986). The microbial world. 5th ed. Prentice-Hall, Englewood Cliffs, N.J.
Shuter, B. (1979). A model of physiological adaptation in unicellular algae. J. theor. Biol. 78: 519–552
Topinka, J. A. (1978). Nitrogen uptake by Fucus spiralis (Phaeophyceae). J. Phycol. 14: 241–247
Author information
Authors and Affiliations
Additional information
Communicated by J. P. Grassle, Woods Hole
Rights and permissions
About this article
Cite this article
Duke, C.S., Litaker, W. & Ramus, J. Effect of temperature on nitrogen-limited growth rate and chemical composition of Ulva curvata (Ulvales: Chlorophyta). Marine Biology 100, 143–150 (1989). https://doi.org/10.1007/BF00391953
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00391953