ESTONIAN ACADEMY
PUBLISHERS
eesti teaduste
akadeemia kirjastus
cover
Estonian Journal of Ecology
Effect of salinity on the growth rate and nutrient stoichiometry of two Baltic Sea filamentous cyanobacterial species; pp. 55–70
PDF | doi: 10.3176/eco.2014.2.01

Authors
Aimar Rakko, Jukka Seppälä
Abstract

Summer blooms of nitrogen-fixing filamentous cyanobacteria are recurrent phenomena in the Baltic Sea. Salinity, varying from 0 to10 PSU in the surface layer of the Baltic Sea, is among the major factors affecting the basin-scale distribution of various bloom-forming cyanobacterial species. The effects of salinity on the growth rate and cellular carbon, nitrogen, and phosphorus ratios of two major cyanobacterial species that form dense blooms in the Baltic, Aphanizomenon sp. (strain KAC 15) and Nodularia spumigena (strain HEM), were studied. Cells were grown under N2-fixing conditions in a salinity gradient from 0 to 10 PSU. The growth rates of the species showed contrasting responses to salinity. For Aphanizomenon sp. the maximum growth rates (0.28–0.31 d–1) were observed at salinities of 0–2 PSU, while for N. spumigena the maximum growth rate occurred at 8–10 PSU (0.14–0.16 d–1). The latter species did not tolerate low salinities (< 2 PSU). The observed differences in salinity tolerances constrain the distribution patterns of these two species during cyanobacterial blooms, Aphanizomenon sp. being more abundant in the coastal and less saline areas. The variations in growth rates were largely reflected in cellular N : P and C : P ratios, which varied two-fold, and in C : Chla ratios with 5-fold variability. Cellular C : N ratios were rather constant at all salinities and close to the Redfield ratio for Aphanizomenon sp. (on average 5.9 g g–1) and above the Redfield ratio for N. spumigena (on average 8.0 g g–1). The relatively higher N : P and lower C : N ratio showed a higher need of N for Aphanizomenon sp. than for N. spumigena. This is partly explained by the higher abundance of N-rich phycobilin pigments in Aphanizomenon sp. as indicated by fluorescence measurements. The observed differences in pigmentation indicate species-specific strategies in light harvesting.

References

Bianchi, T. S., Westman, P. S., Rolff, C., Engelhaupt, E., and Andren, T. 2000. Cyanobacterial blooms in the Baltic Sea: natural or human-induced? Limnology and Oceanography, 45, 716–726.
http://dx.doi.org/10.4319/lo.2000.45.3.0716

Blackburn, S. I., McCausland, M. A., Bolch, C. J. S., Newman, S. J., and Jones, G. J. 1996. Effect of salinity on growth and toxin production in cultures of the bloom-forming cyanobacterium Nodularia spumigena from Australian waters. Phycologia, 35, 511–522.
http://dx.doi.org/10.2216/i0031-8884-35-6-511.1

Gallon, J. R., Evans, A. M., Jones, D. A., Albertano, P., Congesti, R., Bergman, B., et al. 2002. Maximum rates of N2 fixation and primary production are out of phase in a developing cyanobacterial bloom in the Baltic Sea. Limnology and Oceanography, 47, 1514–1521.
http://dx.doi.org/10.4319/lo.2002.47.5.1514

Granéli, E., Wallström, K., Larsson, U., Granéli, W., and Elmgren, R. 1990. Nutrient limitation of primary production in the Baltic Sea area. Ambio, 19, 142–151.

Haney, J. F. 1987. Field studies on zooplankton–cyanobacteria interactions. New Zealand Journal of Marine and Freshwater Research, 21, 467–475.
http://dx.doi.org/10.1080/00288330.1987.9516242

Hense, I. 2007. Regulative feedback mechanisms in cyanobacteria-driven systems: a model study. Marine Ecology Progress Series, 339, 41–47.
http://dx.doi.org/10.3354/meps339041

Hense, I. and Burchard, H. 2010. Modelling cyanobacteria in shallow coastal seas. Ecological Modelling, 221, 238–244.
http://dx.doi.org/10.1016/j.ecolmodel.2009.09.006

Hobson, P. and Fallowfield, H. J. 2001. Effect of salinity on photosynthetic activity of Nodularia spumigena. Journal of Applied Phycology, 13, 493–499.
http://dx.doi.org/10.1023/A:1012540928506

Hobson, P. and Fallowfield, H. J. 2003. Effect of irradiance, temperature and salinity on growth and toxin production by Nodularia spumigena. Hydrobiologia, 493, 7–15.
http://dx.doi.org/10.1023/A:1025447318487

Hobson, P., Fallowfield, H. J., and Burch, M. B. 1999. Effect of total dissolved solids and irradiance on growth and toxin production by Nodularia spumigena. Journal of Applied Phycology, 11, 551–558.
http://dx.doi.org/10.1023/A:1008193918189

Howarth, R. W. and Cole, J. J. 1985. Molybdenum availability, nitrogen limitation, and phyto­plankton growth in natural waters. Science, 229, 653–655.
http://dx.doi.org/10.1126/science.229.4714.653

Howarth, R. W., Marino, R., Lane, J., and Cole, J. J. 1988. Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnology and Oceanography, 33, 688–701.
http://dx.doi.org/10.4319/lo.1988.33.4_part_2.0669

Janson, S. and Granéli, E. 2002. Phylogenetic analyses of nitrogen-fixing cyanobacteria from the Baltic Sea reveal sequence anomalies in the phycocyanin operon. International Journal of Systematic and Evolutionary Microbiology, 52, 1397–1404.
http://dx.doi.org/10.1099/ijs.0.02111-0

Jespersen, A. M. and Christoffersen, K. 1987. Measurements of chlorophyll-a from phytoplankton using ethanol as extraction solvent. Archiv für Hydrobiologie, 109, 445–454.

Johnsen, G. and Sakshaug, E. 2007. Biooptical characteristics of PSII and PSI in 33 species (13 pigment groups) of marine phytoplankton, and the relevance for pulse-amplitude-modulated and fast-repetition-rate fluorometry. Journal of Phycology, 43, 1236–1251.
http://dx.doi.org/10.1111/j.1529-8817.2007.00422.x

Jones, G.  J., Bourne, D. G., Blakely, R. L., and Parker, N. S. 1994. A toxic bloom of Nodularia spumigena Mertens in Orielton Lagoon, Tasmania. Australian Journal of Marine and Freshwater Research, 45, 787–800.
http://dx.doi.org/10.1071/MF9940787

Kahru, M., Horstmann, U., and Rud, O. 1994. Satellite detection of increased cyanobacteria blooms in the Baltic Sea: Natural fluctuation or ecosystem change? Ambio, 23, 469–472.

Kahru, M., Savchuk, O. P., and Elmgren, R. 2007. Satellite measurements of cyanobacterial bloom frequency in the Baltic Sea: interannual and spatial variability. Marine Ecology Progress Series, 343, 15–23.
http://dx.doi.org/10.3354/meps06943

Kanoshina, I., Lips, U., and Leppänen, J.-M. 2003. The influence of weather conditions (temperature and wind) on cyanobacterial bloom development in the Gulf of Finland (Baltic Sea). Harmful Algae, 2, 29–41.
http://dx.doi.org/10.1016/S1568-9883(02)00085-9

Kononen, K. and Nõmmann, S. 1992. Spatio-temporal dynamics of the cyanobacterial blooms in the Gulf of Finland, Baltic Sea. In Marine Pelagic Cyanobacteria: Trichodesmium and Other Diazotrophs (Carpenter, E. J., Capone, D., and Rueter, J., eds), pp. 95–113. Kluwer Academic Publishers, Dordrecht.
http://dx.doi.org/10.1007/978-94-015-7977-3_7

Koroleff, F. 1983. Determination of ammonia. In Methods of Seawater Analysis. Second, revised and extended edition (Grasshoff, K., Ehrhardt, M., and Kremling, K., eds), pp. 150–157. Verlag Chemie, New York.

Laamanen, M. J., Forsström, L., and Sivonen, K. 2002. Diversity of Aphanizomenon flos-aquae (cyanobacterium) populations along a Baltic Sea salinity gradient. Applied and Environmental Microbiology, 68, 5296–5303.
http://dx.doi.org/10.1128/AEM.68.11.5296-5303.2002

Larsson, U., Hajdu, S., Walve, J., and Elmgren, R. 2001. Baltic Sea nitrogen fixation estimated from the summer increase in upper mixed layer total nitrogen. Limnology and Oceanography, 46, 811–820.
http://dx.doi.org/10.4319/lo.2001.46.4.0811

Lehtimäki, J., Sivonen, K., Luukkainen, R., and Niemelä, A. I. 1994. The effects of incubation time, temperature, light, salinity, and phosphorus on growth and hepatotoxin production by Nodularia strains. Archiv für Hydrobiologie, 130, 269–282.

Lehtimäki, J., Moisander, P., Sivonen, K., and Kononen, K. 1997. Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Applied and Environmental Microbiology, 63, 1647–1656.

Lignell, R., Seppälä, J., Kuuppo, P., Tamminen, T., Andersen, T., and Gismervik, I. 2003. Beyond bulk properties: responses of coastal summer plankton communities to nutrient enrichment in the northern Baltic Sea. Limnology and Oceanography, 48,189–209.
http://dx.doi.org/10.4319/lo.2003.48.1.0189

Lukatelich, R. J. and McComb, A. J. 1986. Nutrient levels and the development of diatom and blue-green algal blooms in a shallow Australian estuary. Journal of Plankton Research, 8, 597–618.
http://dx.doi.org/10.1093/plankt/8.4.597

Moisander, P. H., Hench, J. L., Kononen, K., and Paerl, H. W. 2002. Small-scale shear effects on heterocystous cyanobacteria. Limnology and Oceanography, 47, 108–119.
http://dx.doi.org/10.4319/lo.2002.47.1.0108

Niemi, Å. 1979. Blue-green algal blooms and N : P ratio in the Baltic Sea. Acta Botanica Fennica, 110, 57–61.

Niemistö, L., Rinne, I., Melvasalo, T., and Niemi, Å. 1989. Blue-green algae and their nitrogen fixation in the Baltic Sea in 1980, 1982 and 1984. Meri, 17, 1–59.

Nordin, R. N. and Stein, J. R. 1980. Taxonomic revision of Nodularia (Cyanophyceae/Cyanobacteria). Canadian Journal of Botany, 58, 1212–1224.
http://dx.doi.org/10.1139/b80-151

Oliver, R. L. 1994. Floating and sinking in gas-vacuolate cyanobacteria. Journal of Phycology, 30, 161–173.
http://dx.doi.org/10.1111/j.0022-3646.1994.00161.x

Osgood, R. A. 1988. A hypothesis on the role of Aphanizomenon in translocating phosphorus. Hydrobiologia, 169, 69–76.
http://dx.doi.org/10.1007/BF00007934

Paerl, H. W. 2000. Marine plankton. In The Ecology of Cyanobacteria (Whitton, B. A. and Potts, M., eds), pp. 121–148. Kluwer Academic Publishers, Dordrecht.

Pettersson, K., Herlitz, E., and Istvanovics, V. 1993. The role of Gloeotrichia echinulata in the transfer of phosphorus from sediments to water in Lake Erken. Hydrobiologia, 253, 123–129.
http://dx.doi.org/10.1007/BF00050732

Raateoja, M., Kuosa, H., and Haellfors, S. 2011. Fate of excess phosphorus in the Baltic Sea: A real 25 driving force for cyanobacterial blooms? Journal of Sea Research, 65, 315–321.
http://dx.doi.org/10.1016/j.seares.2011.01.004

Redfield, A. 1958. The biological control of chemical factors in the environment. American Scientist, 46, 205­–221.

Seppälä, J., Ylöstalo, P., Kaitala, S., Hällfors, S., Raateoja, M., and Maunula, P. 2007. Ship-of opportunity based phycocyanin fluorescence monitoring of the filamentous cyanobacteria bloom dynamics in the Baltic Sea. Estuarine, Coastal and Shelf Science, 73, 489–500.
http://dx.doi.org/10.1016/j.ecss.2007.02.015

Sivonen, K., Kononen, K., Carmichael, W. W., Dahlem, A. M., Rinehart, K. L., Kiviranta, J., and Niemelä, S. I. 1989. Occurrence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and structure of the toxin. Applied and Environmental Microbiology, 55, 1990–1995.

Smith, V. H. 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science, 221, 669–671.
http://dx.doi.org/10.1126/science.221.4611.669

Solorzano, L. and Sharp, J. H. 1980. Determination of total dissolved phosphorus and particulate phosphorus in natural waters. Limnology and Oceanography, 25, 754–758.
http://dx.doi.org/10.4319/lo.1980.25.4.0754

Stal, L. J., Staal, M., and Villbrandt, M. 1999. Nutrient control of cyanobacterial blooms in the Baltic Sea. Aquatic Microbial Ecology, 18, 165–173.
http://dx.doi.org/10.3354/ame018165

Stal, L. J., Albertano, P., Bergman, B., von Bröckel, K., Gallon, J. R., Hayes, P. K., et al. 2003. BASIC: Baltic Sea cyanobacteria. An investigation of the structure and dynamics of water blooms of cyanobacteria in the Baltic Sea – responses to a changing environment. Continental Shelf Research, 23, 1695–1714.
http://dx.doi.org/10.1016/j.csr.2003.06.001

Stipa, T. 2002. Temperature as a passive isopycnal tracer in salty spiceless oceans. Geophysical Research Letters, 7, 335–342.

Turpin, D. H., Layzell, D. B., and Elrifi, I. R. 1985. Modeling the C economy of Anabaena flos-aqua. Plant Physiology, 78, 746–752.
http://dx.doi.org/10.1104/pp.78.4.746

Vahtera, E., Laanemets, J., Pavelson, J., Huttunen, M., and Kononen, K. 2005. Effect of upwelling on the pelagic environment and bloom-forming cyanobacteria in the western Gulf of Finland, Baltic Sea. Journal of Marine Systems, 58, 67–82.
http://dx.doi.org/10.1016/j.jmarsys.2005.07.001

Vahtera, E., Conley, D., Gustafsson, B. G., Kuosa, H., Pitkänen, H., Savchuk, O. P., et al. 2007. Internal ecosystem feedbacks enhance nitrogen-fixing cyanobacteria blooms and complicate management in the Baltic Sea. Ambio, 36, 186–194.
http://dx.doi.org/10.1579/0044-7447(2007)36[186:IEFENC]2.0.CO;2

Vonshak, A. and Tomaselli, L. 2000. Arthrospira (Spirulina): systematics and ecophysiology. In The Ecology of Cyanobacteria (Whitton, B. A. and Potts, M., eds), pp. 505–522. Kluwer Academic Publishers, Dordrecht.

Wasmund, N. 1997. Occurrence of cyanobacterial blooms in the Baltic Sea in relation to environ­mental conditions. Internationale Revue der Gesamten Hydrobiologie, 82, 169–184.
http://dx.doi.org/10.1002/iroh.19970820205

Wulff, F., Stigebrandt, A., and Rahm, L. 1990. Nutrient dynamics of the Baltic Sea. Ambio, 19, 126–133.

Back to Issue

Back issues