Skip to main content
Log in

Impact of temperature and species interaction on filamentous cyanobacteria may be more important than salinity and increased pCO2 levels

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

A future business-as-usual scenario (A1FI) was tested on two bloom-forming cyanobacteria of the Baltic Proper, Nodularia spumigena and Aphanizomenon sp., growing separately and together. The projected scenario was tested in two laboratory experiments where (a) interactive effects of increased temperature and decreased salinity and (b) interactive effects of increased temperature and elevated levels of pCO2 were tested. Increased temperature, from 12 to 16 °C, had a positive effect on the biovolume and photosynthetic activity (F v/F m) of both species. Compared when growing separately, the biovolume of each species was lower when grown together. Decreased salinity, from 7 to 4, and elevated levels of pCO2, from 380 to 960 ppm, had no effect on the biovolume, but on F v/F m of N. spumigena with higher F v/F m in salinity 7. Our results suggest that the projected A1FI scenario might be beneficial for the two species dominating the extensive summer blooms in the Baltic Proper. However, our results further stress the importance of studying interactions between species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andersson A, Haecky P, Hagström Å (1994) Effect of temperature and light on the growth of micro- nano- and pico-plankton: impact on algal succession. Mar Biol 120:511–520

    Article  Google Scholar 

  • Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622

    Article  CAS  Google Scholar 

  • Barker GLA, Konopka A, Handley BA, Hayes PK (2000) Genetic variation in Aphanizomenon (Cyanobacteria) colonies from the Baltic Sea and North America. J Phycol 36:947–950

    Article  CAS  Google Scholar 

  • Blackburn SI, McCausland MA, Bolch CJS, Newman SJ, Jones GJ (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

    Article  Google Scholar 

  • Borges AV, Frankignoulle M (1999) Daily and seasonal variations of the partial pressure of CO2 in surface seawater along Belgian and southern Dutch coastal areas. J Mar Syst 19:251–266

    Article  Google Scholar 

  • Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62:667–683

    CAS  Google Scholar 

  • Chierici M, Fransson A, Anderson LG (1999) Influence of m-cresol purple indicator additions on the pH of seawater samples: correction factors evaluated from a chemical speciation model. Mar Chem 65:281–290

    Article  CAS  Google Scholar 

  • Clayton TD, Byrne RH (1993) Spectrophotometric seawater pH measurements—total hydrogen-ion concentration scale calibration of m-cresol purple and at-sea results. Deep-Sea Res I 40:2115–2129

    Article  CAS  Google Scholar 

  • Cosgrove J, Borowitzka M (2006) Applying pulse amplitude modulation (PAM) fluorometry to microalgae suspensions: stirring potentially impacts fluorescence. Photosynth Res 88:343–350

    Article  CAS  Google Scholar 

  • Cox PA, Banack SA, Murch SJ et al (2005) Diverse taxa of cyanobacteria produce beta-N-methylamino-l-741 alanine, a neurotoxic amino acid. PNAS 102:5074–5078

    Article  CAS  Google Scholar 

  • Dickson AG (1990) Standard potential of the reaction: AgCl(s) + OH2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO4 in synthetic seawater from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127

    Article  CAS  Google Scholar 

  • Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res Pt I 34:1733–1743

    Article  CAS  Google Scholar 

  • Edler L (1979) Phytoplankton succession in the Baltic Sea. Acta Bot Fennica 110:75–78

    Google Scholar 

  • Fischlin A, Midgley GF, Price JT et al (2007) Ecosystems, their properties, goods, and services. In: Parry ML, Canziani OF, Palutikof JP et al (eds) Climate change 2007: impacts, adaptation and vulnerability. Contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change, Cambridge University Press, Cambridge and New York

  • Fransson A, Chierici M, Anderson LG (2004) Diurnal variability in the oceanic carbon dioxide system and oxygen in the Southern Ocean surface water. Deep Sea Res II 51:2827–2839

    Article  CAS  Google Scholar 

  • Fu F-X, Warner ME, Zhang Y, Feng Y, Hutchins DA (2007) Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (cyanobacteria). J Phycol 43:485–496

    Article  Google Scholar 

  • Gattuso JP, Gao K, Lee K, Rost B, Schulz KG (2010) Approaches and tools to manipulate the carbonate chemistry. In: Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg

    Google Scholar 

  • Granéli E, Johansson N, Panosso R (1998) Cellular toxin contents in relation to nutrient conditions for different groups of phycotoxins. In: Reguera B, Blanco J, Fernéndez ML, Wyatt T (eds) Harmful algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO Paris, France, pp 321–324

    Google Scholar 

  • Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of seawater analysis, 3rd edn. Wiley-VHC, Weinheim

    Book  Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 29–60

    Chapter  Google Scholar 

  • Hagström Å, Larsson U (1984) Diel and seasonal variation in growth rates of pelagic bacteria. In: Hobbie JE, Williams PJ (eds) Heterotrophic activity in the sea. Plenum Press, New York, pp 249–262

    Chapter  Google Scholar 

  • Haraldsson C, Anderson LG, Hassellöv M, Hulth S, Olsson K (1997) Rapid, high-precision potentiometric titration of alkalinity in the ocean and sediment pore waters. Deep-Sea Res I 44:2031–2044

    Article  CAS  Google Scholar 

  • Havenhand JN (2012) How will ocean acidification affect Baltic Sea ecosystems? An assessment of plausible impacts on key functional groups. AMBIO 41:637–644

    Google Scholar 

  • Hayes PK, Barker GLA, Batley J et al (2002) Genetic diversity within populations of cyanobacteria assessed by analysis of single filaments. Antonie Leeuwenhoek 81:197–202

    Article  CAS  Google Scholar 

  • HELCOM (2007) Climate change in the Baltic Sea area—HELCOM thematic assessment 2007. Baltic Sea environment proceedings no. 111

  • Hobson P, Burch M, Fallowfield HJ (1999) Effect of total dissolved solids and irradiance on growth and toxin production by Nodularia spumigena. J Appl Phycol 11:551–558

    Article  CAS  Google Scholar 

  • Hutchins DA, Fu FX, Zhang Y et al (2007) CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol Oceanogr 53:1293–1304

    Article  Google Scholar 

  • Ibelings BW, Havens KE (2008) Cyanobacterial toxins: a qualitative meta-analysis of concentrations, dosage and effects in freshwater, estuarine and marine biota. In: Hudnell HK (ed) Cyanobacterial harmful algal blooms: state of the science and research needs, vol 619. Springer, Berlin, pp 675–732

    Chapter  Google Scholar 

  • Janson S, Hayes PK (2006) Molecular taxonomy of harmful algae. In: Granéli E, Turner JT (eds) Ecology of harmful algae. Ecological studies, vol 189. Springer, Berlin, pp 9–21

    Chapter  Google Scholar 

  • Johnson VR, Brownlee C, Rickaby REM et al (2011) Responses of marine benthic microalgae to elevated CO2. Mar Biol. doi:10.1007/s00227-011-1840-2

    Google Scholar 

  • Jonasson S (2006) Monitoring the cellular phosphate status in bloom-forming cyanobacteria of the Baltic Sea. Dissertation, Stockholm University

  • Kanoshina I, Lips U, 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

    Article  Google Scholar 

  • Karjalainen M, Engström-Öst J, Korpinen S et al (2007) Ecosystem consequences of cyanobacteria in the Northern Baltic Sea. AMBIO 36:195–202

    Article  CAS  Google Scholar 

  • Kim HC, Lee K (2009) Significant contribution of dissolved organic matter to seawater alkalinity. Geophys Res Lett 36. doi:10.1029/2009GL040271

  • Kranz SA, Levitan O, Richter KU et al (2010) Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: physiological responses. J Plant Physiol 154:334–345

    Article  CAS  Google Scholar 

  • Laamanen MJ, Gugger MF, Lehtimäki JM, Haukka K, Sivonen K (2001) Diversity of toxic and nontoxic Nodularia isolates (Cyanobacteria) and filaments from the Baltic Sea. Appl Environ Microbiol 67:4638–4647

    Article  CAS  Google Scholar 

  • Laamanen MJ, Forsström L, Sivonen K (2002) Diversity of Aphanizomenon flos-aquae (Cyanobacterium) populations along a Baltic Sea salinity gradient. Appl Environ Microbiol 68:5296–5303

    Article  CAS  Google Scholar 

  • Legrand C, Rengefors K, Fistarol GO, Granéli E (2003) Allelopathy in phytoplankton—biochemical, ecological and evolutionary aspects. Phycologia 42:406–419

    Article  Google Scholar 

  • Lehtimäki J, Sivonen K, Luukainen R, Niemela SI (1994) The effects of incubation time, temperature, light, salinity, and phosphorus on growth and hepatotoxin production by Nodularia strains. Arch Hydrobiol 130:269–282

    Google Scholar 

  • Lehtimäki J, Moisander P, Sivonen K, Kononen K (1997) Growth, nitrogen fixation and nodularin production by two Baltic Sea cyanobacteria. Symbiosis 6:181–194

    Google Scholar 

  • Mazur-Marzec H, Zeglinska L, Plinski M (2005) The effect of salinity on the growth, toxin production, and morphology of Nodularia spumigena isolated from the Gulf of Gdansk, southern Baltic Sea. J Appl Phycol 17:171–179

    Article  CAS  Google Scholar 

  • Meehl GA, Stocker TF, Collins WD et al (2007) Global climate projections. In: Solomon S, Qin D, Manning M et al (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change, Cambridge University Press, Cambridge and New York

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    Article  CAS  Google Scholar 

  • Mohlin M, Wulff A (2009) Interaction effects of ambient UV radiation and nutrient limitation on the toxic cyanobacterium Nodularia spumigena. Microb Ecol 57:675–686

    Article  Google Scholar 

  • Mohlin M, Roleda MY, Pattanaik B, Tenne S-J, Wulff A (2012) Interspecific resource competition—combined effects of radiation and nutrient limitation on two diazotrophic filamentous cyanobacteria. Microb Ecol 63:736–750

    Google Scholar 

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

    CAS  Google Scholar 

  • Pattanaik B, Wulff A, Roleda MY, Garde K, Mohlin M (2010) Production of the cyanotoxin nodularin—a multifactorial approach. Harmful Algae 10:30–38

    Article  CAS  Google Scholar 

  • Pierrot D, Lewis E, Wallace DWR (2006) MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, TN

  • Pliński M, Jόźwiak T (1999) Temperature and N:P ratio as factors causing blooms of blue-green algae in the Gulf of Gdańsk. Oceanologia 41:73–80

    Google Scholar 

  • Ploug H (2008) Cyanobacterial surface blooms formed by Aphanizomenon sp. and Nodularia spumigena in the Baltic Sea: small-scale fluxes, pH, and oxygen microenvironments. Limnol Oceanogr 53:914–921

    Article  CAS  Google Scholar 

  • Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23:187–204

    Article  Google Scholar 

  • Poza-Carrión C, Fernández-Valiente E, Fernández Piñas F, Leganés F (2001) Acclimation of photosynthetic pigments and photosynthesis of the cyanobacterium Nostoc sp. strain UAM206 to combined fluctuations of irradiance, pH, and inorganic carbon availability. J Plant Physiol 158:1455–1461

    Article  Google Scholar 

  • Raven JA, Beardall J (2003) Carbon acquisition mechanisms in algae: carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in Algae. Kluwer, Dordrecht, pp 225–244

    Chapter  Google Scholar 

  • Raven J, Caldeira K, Elderfield H et al (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy document 12/05 by The Royal Society, London

  • Repka S, Mehtonen J, Vaitomaa J, Saari L, Sivonen K (2001) Effects of nutrients on growth and nodularin production of Nodularia strain GR8b. Microb Ecol 42:606–613

    Article  CAS  Google Scholar 

  • Roleda MY, Mohlin M, Pattanaik B, Wulff A (2008) Photosynthetic response of Nodularia spumigena to UV and photosynthetically active radiation depends on nutrient (N, P) availability. FEMS Microbiol Ecol 66:230–242

    Article  CAS  Google Scholar 

  • Schlüter L, Lutnaes BF, Liaaen-Jensen S et al (2008) Correlation of the content of hepatotoxin nodularin and glycosidic carotenoids, 4-ketomyxol- 2′-fucoside and novel 1′-O-methyl-4-ketomyxol-2′-fucoside, in 20 strains of the cyanobacterium Nodularia spumigena. Biochem Syst Ecol 36:749–757

    Article  Google Scholar 

  • Sellner KG (1997) Physiology, ecology, and toxic properties of marine cyanobacteria blooms. Limnol Oceanogr 42:1089–1104

    Article  Google Scholar 

  • Shiah FK, Ducklow HW (1994) Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate in Chesapeake Bay. Limnol Oceanogr 39:1243–1258

    Article  Google Scholar 

  • Sipiä VO, Kankaanpaa HT, Pflugmacher S, Flinkman J, Furey A, James KJ (2002) Bioaccumulation and detoxication of nodularin in tissues of flounder (Platichthys flesus), mussels (Mytilus edulis, Dreissena polymorpha), and clams (Macoma balthica) from the northern Baltic Sea. Ecotoxicol Environ Saf 53:305–311

    Article  Google Scholar 

  • Suikkanen S, Fistarol GO, Granéli E (2004) Allelopathic effects of the Baltic cyanobacteria Nodularia spumigena, Aphanizomenon flos-aque and Anabaena lemmermannii on algal monocultures. J Exp Mar Biol Ecol 308:85–101

    Article  Google Scholar 

  • Suikkanen S, Fistarol GO, Granéli E (2005) Effects of cyanobacterial allelochemicals on a natural plankton community. Mar Ecol Prog Ser 287:1–9

    Article  Google Scholar 

  • Suikkanen S, Engström-Öst J, Jokela J, Sivonen K, Viitasalo M (2006) Allelopathy of Baltic Sea cyanobacteria: no evidence for the role of nodularin. J Plankton Res 28:543–550

    Article  CAS  Google Scholar 

  • Torstensson A, Chierici M, Wulff A (2012) The influence of temperature and carbon dioxide levels on the benthic/sea ice diatom Navicula directa. Polar Biol 35:205–214

    Article  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge

    Google Scholar 

  • Wrona FJ, Prowse TD, Reist JD et al (2006) Climate change effects on aquatic biota, ecosystem structure and function. AMBIO 35:359–369

    Article  CAS  Google Scholar 

  • Wulff A, Mohlin M, Sundbäck K (2007) Intraspecific variation in the response of the cyanobacterium Nodularia spumigena to moderate UV-B radiation. Harmful Algae 6:388–399

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was financed by Magnus Bergvall Foundation and Oscar and Lili Lamm Foundation. We thank M. Appelgren, M. Mohlin, A. Torstensson and K. Vikström for assistance in the laboratory. We are grateful to J. Havenhand, S. Dupont and an anonymous reviewer for constructive criticism, improving an earlier version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Karlberg.

Additional information

Communicated by S. Dupont.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karlberg, M., Wulff, A. Impact of temperature and species interaction on filamentous cyanobacteria may be more important than salinity and increased pCO2 levels. Mar Biol 160, 2063–2072 (2013). https://doi.org/10.1007/s00227-012-2078-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-012-2078-3

Keywords

Navigation