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Growth, nutrient uptake capacities and tissue constituents of the macroalgae Cladophora vagabunda and Gracilaria tikvahiae related to site-specific nitrogen loading rates

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Abstract

Cladophora vagabunda (L.) van den Hoek and Gracilaria tikvahiae (McLachlan) have become dominant components of the macroalgal assemblage in Waquoit Bay, a Massachusetts embayment, possibly due to nitrogen (N) enrichment from anthropogenic inputs transported via groundwater. During 1989–1993, we measured site-related growth, ammonium uptake rates and tissue constituents of these macroalgae from areas subject to high N loading rates (Childs River) and lower N loadings rates (Sage Lot Pond). We also conducted in situ and microcosm enrichment experiments to determine what limited algal growth throughout the year. Our results indicated that these species are strongly affected by and have a strong impact on the N environment of this embayment. For example, C. vagabunda and G. tikvahiae from Childs River had higher light-harvesting pigments and tissue-N concentrations than Sage Lot Pond populations. Additionally, both Childs River populations showed greater site-specific growth and N uptake rates, particularly during the summer period of peak growth. In fact, maximum uptake rates of 90 and over 140 μmol dry wt g-1 h-1 for Childs River C. vagabunda and G. tikvahiae, respectively, suggest that these species can remove substanital quantities of N from overlying waters, and may be responsible for low (often (<1 μM) water-column nutrient concentrations during summer. In situ and tank enrichment experiments indicated that growth rates were limited by available N during summer, while P may be limiting during a brief period toward the end of the annual growth cycle (autumn). Under experimental enrichment, growth rates of Sage Lot Pond algae were similar to values measured at the site receiving higher N inputs, and generally, G. tikvahiae showed growth enhancement (up to 0.2 doublings d-1) under light-saturating conditions (0.5 m) while C. vagabunda showed nutrient-enhanced growth at 2.5 m. The effects of available nutrients on algal growth were strongly influenced by irradiance and temperature, resulting in a complex seasonal interaction that emphasized the dynamic nature of species response to N loading. Dominance by these two macroalgae in Waquoit Bay, as in other areas undergoing eutrophication, is likely related to physiological strategies that enable these species to tolerate large environmental variations, to take advantage of greater N availability and to survive indirect effects of N loading (e.g. reduced irradiance, anoxia).

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References

  • Bach SD, Josselyn MN (1978) Mass blooms of the alga Cladophora in Bermuda. Mar Pollut Bull 9:34–37

    Google Scholar 

  • Bach SD, Josselyn MN (1979) Production and biomass of Cladophora prolifera (Chlorophyta, Cladophorales) in Bermuda. Bot mar 22:163–168

    Google Scholar 

  • Birch PB, Gordon DM, McComb AJ (1981) Nitrogen and phosphorus nutrition of Cladophora in the Peel-Harvey system, western Australia. Bot mar 24:381–387

    Google Scholar 

  • Bird KT, Habig C, DeBusk T (1982) Nitrogen allocation and storage patterns in Gracilaria tikvahiae (Rhodophyta). J Phycol 18:344–348

    Google Scholar 

  • Bower CE, Holm-Hansen T (1980) A salicylate-hypochloride method for determining ammonia in seawater. Can J Fish aquat Sciences 37:794–798

    Google Scholar 

  • Cambridge ML, Breeman AM, van den Hoek C (1990) Temperature limits at the distribution boundaries of four tropical to temperate species of Cladophora (Cladophorales: Chlorophyta) in the North Atlantic Ocean. Aquat Bot 38:135–151

    Google Scholar 

  • Capone DG, Bautista, MF (1985) A groundwater source of nitrate in nearshore marine sediments. Nature, Lond 313:214–216

    Google Scholar 

  • Cloern JE (1982) Does the benthos control phytoplankton biomass in south San Francisco Bay. Mar Ecol Prog Ser 9:191–202

    Google Scholar 

  • Curley J, Lawton R, Hickey J, Friske J (1971) A study of the marine resources of the Waquoit Bay-Eel Pond Estuary. Mass Div mar Fish Monogr Ser 9:1–40

    Google Scholar 

  • Dawes CJ, Koch EW (1990) Physiological responses of the red algae Gracilaria verrucosa and G. tikvahiae before and nutrient enrichment. Bull mar Sci 46:335–344

    Google Scholar 

  • Day RW, Quinn GP (1989) Comparisons of treatments after an analysis of variance in ecology. Ecol Monogr 59:433–463

    Google Scholar 

  • DeBoer JA, Guigi HJ, Israel TL, D'Elia CF (1978) Nutritional studies of two red algae. I. Growth rate as a function of nitrogen source and concentration. J Phycol 14:261–266

    Google Scholar 

  • D'Elia CF, DeBoer JA (1978) Nutritional studies of two red algae. II. Kinetics of ammonium and nitrate uptake. J Phycol 14: 266–272

    Google Scholar 

  • D'Elia CF, Sanders JG, Boynton WR (1986) Nutrient enrichment studies in a coastal plain estuary: phytoplankton growth in large-scale continuous cultures. Can J Fish aquat Sciences 43:397–406

    Google Scholar 

  • Duncan MJ, Harrison PJ (1982) Comparison of solvents for extracting chlorophylls from marine macrophytes. Bot mar 25: 445–447

    Google Scholar 

  • Fisher TR, Peele ER, Ammerman JW, Harding Jr LW (1992) Nutrient limitation of phytoplankton in Chesapeake Bay. Mar Ecol Prog Ser 82:51–63

    Google Scholar 

  • Fujita RM (1985) The role of nitrogen status in regulation transient ammonium uptake and nitrogen storage by macroalgae. J exp mar Biol Ecol 92:283–301

    Google Scholar 

  • Gordon DM, Birch PM, McComb AJ (1980) The effect of light, temperature, and salinity on photosynthetic rates of an estuarine Cladophora. Bot mar 23:749–755

    Google Scholar 

  • Gordon DM, Birch PB, McComb AJ (1981) Effects of inorganic phosphorus and nitrogen on the growth of an estuarine Cladophora in culture. Bot mar 24:93–106

    Google Scholar 

  • Haberstroh SC (1990) The response of natural phytoplankton populations to nutrient loading in Waquoit Bay, Cape Cod. Senior thesis, Smith College, Northampton, Massachusetts

    Google Scholar 

  • Hanisak MD (1983) The nitrogen relationships of marine macroalgae. In: Carpenter EG, Capone DG (eds) Nitrogen in the marine environment. Academic Press, New York, pp 699–730

    Google Scholar 

  • Harlin MM, Thorne-Miller B (1981) Nutrient enrichment of seagrass beds in a Rhode Island coastal lagoon. Mar Biol 65:221–229

    Google Scholar 

  • Harlin MM, Thorne-Miller B, Thursby GB (1977) Ammonium uptake by Gracilaria sp. (Florideophyceae) and Ulva lactuca (Chlorophyceae) in closed system fish culture. Proc. 9th int. Seaweed Symp. 9:285–295 [Jensen J, Stein JR (ed) Science Press, Princeton]

    Google Scholar 

  • Howarth RW (1988) Nutrient limitation of net primary production in marine ecosystems. A Rev Ecol Syst 19:89–110

    Google Scholar 

  • Kautsky L (1982) Primary production and uptake kinetics of ammonium and phosphate by Enteromorpha compressa in an ammonium sulfate industry outlet area. Aquat Bot 12:23–40

    Google Scholar 

  • Lapointe BE (1987) Phosphorus-and nitrogen-limited photosynthesis and growth of Gracilaria tikvahiae (Rhodophyceae) in the Florida Keys: an experimental field study. Mar Biol 93:561–568

    Google Scholar 

  • Lapointe BE, Clark MW (1992) Nutrient inputs from the watershed and coastal eutrophication in the Florida Keys. Estuaries 15:465–476

    Google Scholar 

  • Lapointe BE, Duke CS (1984) Biochemical strategies for growth of Gracilaria tikvahiae (Rhodophyta) in relation to light intensity and nitrogen availability. J Phycol 20:488–495

    Google Scholar 

  • Lapointe BE, Littler MM, Littler DS (1992) Nutrient availability to marine macroalgae in siliciclastic versus carbonate-rich coastal waters. Estuaries 15:75–82

    Google Scholar 

  • Lapointe BE, O'Connell J (1989) Nutrient-enhanced growth of Cladophora prolifera in Harrington Sound, Bermuda: eutrophication of a confined, phosphorus-limited marine ecosystem. Estuar cstl Shelf Sci 28:347–360

    Google Scholar 

  • Lavery PS, Lukatelich RJ, McComb AJ (1991) Changes in the biomass and species composition of macroalgae in a eutrophic estuary. Estuar cstl Shelf Sci 33:1–22

    Google Scholar 

  • Lavery PS, McComb AJ (1991) The nutritional eco-physiology of Chaetomorpha linum and Ulva rigida in Peel Inlet, Western Australia. Bot mar 34:251–260

    Google Scholar 

  • Lee V, Olsen S (1985) Eutrophication and management initiatives for the control of nutrient inputs to Rhode Island coastal lagoons. Estuaries 8:191–202

    Google Scholar 

  • Maldonado M (1990) Effect of disparate nitrogen loading rates on nutrient uptake and tissue constituents of two nuisance macroalgal species, Gracilaria tikvahiae and Cladophora vagabunda. Senior thesis, Smith College, Northampton, Massachusetts

    Google Scholar 

  • Menzel DW, Corwin N (1965) The measurement of total phosphorus in seawater based on the liberation of organically bound fractions by persulfate oxidation. Limnol Oceanogr 10:280–282

    Google Scholar 

  • Nichols FH, Cloern JE, Luoma SN, Peterson DH (1986) The modification of an estuary. Science, NY 231:567–573

    Google Scholar 

  • Nixon SW, Oviatt CA, Frithsen J, Sullivan B (1986) Nutrients and the productivity of estuarine and coastal marine ecosystems. J Limnol Soc Sth Afr 12:43–71

    Google Scholar 

  • Nixon S, Pilson M (1983) Nitrogen in estuarine and coastal marine ecosystems. In: Carpenter FG, Capone, DG (eds) Nitrogen in the marine environment. Academic Press, New York, pp 565–648

    Google Scholar 

  • Oviatt CA, Keller AA, Sampou PA, Beatty LL (1986) Patterns of productivity during a mesocosm experiment. Mar Ecol Prog Ser 28:69–80

    Google Scholar 

  • Oviatt CA, Quinn JG, Maughan JT, Ellis JT, Sullivan KB, Gearing JN, Gearing PJ, Hunt CD, Sampou PA, Latimer JS (1987) Fate and effects of sewage sludge in the coastal marine environment: a mesocosm experiment. Mar Ecol Prog Ser 41:187–203

    Google Scholar 

  • Peckol P, Ramus J (1988) Abundances and physiological properties of deep-water seaweeds from the Carolina outer continental shelf. J exp mar Biol Ecol 115:25–39

    Google Scholar 

  • Persky JH (1986) The relation of groundwater quality to housing density, Cape Cod, Massachusetts. USGS Water Resources Investigation Report 86-4093, Boston, Massachusetts

  • Porra RJ, Thompson WA, Kriedemann DE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Google Scholar 

  • Pregnall AM, Rudy PP (1985) Contributions of green macroalgal mats (Enteromorpha spp.) to seasonal production in an estuary. Mar Ecol Prog Ser 24:167–176

    Google Scholar 

  • Rhee G-Yull (1980) Continuous culture in phytoplankton ecology. In: Droop MR, Jannash HW (eds) Advances in aquatic microbiology. Academic Press, New York, pp 151–203

    Google Scholar 

  • Rosenberg G (1981) Ecological growth strategies in the seaweeds Gracilaria foliifera (Rhodophyceae) and Ulva sp. (Chlorophyceae). Ph D dissertation, Yale University, New Haven, Connecticut

  • Ryther JH, Corwin N, DeBusk TA, Williams LD (1981) Nitrogen uptake and storage by the red alga Gracilaria tikvahiae (McLachlan, 1979). Aquaculture, Amsterdam 26:107–115

    Google Scholar 

  • Ryther JH, Dunstan WM (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science, NY 171: 1008–1013

    Google Scholar 

  • Sanders JG, Cibik SJ, D'Elia CF, Boynton WR (1987) Nutrient enrichment studies in a coastal plain estuary: changes in phytoplankton species composition. Can J Fish aquat Sciences 44: 83–90

    Google Scholar 

  • Schneider SW, Searles RB (1991) Seaweeds of the southern United States. Duke University Press, Durham, North Carolina

    Google Scholar 

  • Shoaf WT, Lium BW (1976) Improved extraction of chlorophyll a and b from algae using dimethyl sulfoxide. Limnol Oceanogr 21:926–928

    Google Scholar 

  • Siegelman HW, Kycia JH (1978) Algal biliproteins. In: Hellebust JA, Craigie JS (eds) Handbook of phycological methods: physiological and biochemical methods. Cambridge University Press, London

    Google Scholar 

  • Sokal RR, Rohlf FL (1981) Biometry: the principles and practice of statistics in biological research, 2nd edn. W. H. Freemann and Company, San Francisco, California

    Google Scholar 

  • Strickland JD, Parsons TR (1972) A practical handbook of seawater analysis. Bull Fish Res Bd Can 167:1–310

    Google Scholar 

  • Taylor WR (1957) Marine algae of the northeastern coast of North America. The University of Michigan Press, Ann Arbor, Michigan

    Google Scholar 

  • Tewari A, Joshi MV (1988) Effect of domestic sewage and industrial effluents on biomass and species diversity of seaweeds. Bot mar 31:389–397

    Google Scholar 

  • Thorne-Miller B, Harin MM, Thursby GB, Brady-Campbell MM, Dworetsky BA (1983) Variations in the distribution and biomass of submerged macrophytes in five coastal lagoons in Rhode Island, U.S.A. Bot mar 26:231–242

    Google Scholar 

  • Valiela I, Costa JE (1988) Eutrophication of Buttermilk Bay, a Cape Cod coastal embayment: concentration of nutrients and watershed nutrient budgets. Envir Mgmt 12:539–553

    Google Scholar 

  • Valiela I, Costa J, Foreman K, Teal JM, Howes B, Aubrey D (1990) Transport of groundwater-borne nutrients from watersheds and their effects on coastal waters. Biogeochemistry (Dordrecht) 10:177–197

    Google Scholar 

  • Valiela I, Foreman K, LaMontagne M, Hersh D, Costa J, Peckol P, DeMeo-Anderson B, D'Avanzo C, Babione M, Sham C-H, Bawley J, Lajtha K (1992) Couplings of watersheds and coastal waters: sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts. Estuaries 15:443–457

    Google Scholar 

  • Wallentinus I (1984) Comparisons of nutrient uptake rates for Baltic macroalgae with different thallus morphologies. Mar biol 80:215–225

    Google Scholar 

  • Yates MV (1985) Septic tank density and ground-water contamination. Ground Water 23:586–591

    Google Scholar 

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Communicated by J. P. Grassle, New Brunswick

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Peckol, P., DeMeo-Anderson, B., Rivers, J. et al. Growth, nutrient uptake capacities and tissue constituents of the macroalgae Cladophora vagabunda and Gracilaria tikvahiae related to site-specific nitrogen loading rates. Marine Biology 121, 175–185 (1994). https://doi.org/10.1007/BF00349487

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