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.
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
Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622
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
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
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
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
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
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
Cosgrove J, Borowitzka M (2006) Applying pulse amplitude modulation (PAM) fluorometry to microalgae suspensions: stirring potentially impacts fluorescence. Photosynth Res 88:343–350
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
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
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
Edler L (1979) Phytoplankton succession in the Baltic Sea. Acta Bot Fennica 110:75–78
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
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
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
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
Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of seawater analysis, 3rd edn. Wiley-VHC, Weinheim
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
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
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
Havenhand JN (2012) How will ocean acidification affect Baltic Sea ecosystems? An assessment of plausible impacts on key functional groups. AMBIO 41:637–644
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
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
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
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
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
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
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
Karjalainen M, Engström-Öst J, Korpinen S et al (2007) Ecosystem consequences of cyanobacteria in the Northern Baltic Sea. AMBIO 36:195–202
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
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
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
Legrand C, Rengefors K, Fistarol GO, Granéli E (2003) Allelopathy in phytoplankton—biochemical, ecological and evolutionary aspects. Phycologia 42:406–419
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
Lehtimäki J, Moisander P, Sivonen K, Kononen K (1997) Growth, nitrogen fixation and nodularin production by two Baltic Sea cyanobacteria. Symbiosis 6:181–194
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
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
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
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
Niemi Å (1979) Blue-green algal blooms and N:P ratio in the Baltic Sea. Acta Bot Fennica 110:57–61
Pattanaik B, Wulff A, Roleda MY, Garde K, Mohlin M (2010) Production of the cyanotoxin nodularin—a multifactorial approach. Harmful Algae 10:30–38
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
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
Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23:187–204
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
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
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
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
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
Sellner KG (1997) Physiology, ecology, and toxic properties of marine cyanobacteria blooms. Limnol Oceanogr 42:1089–1104
Shiah FK, Ducklow HW (1994) Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate in Chesapeake Bay. Limnol Oceanogr 39:1243–1258
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
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
Suikkanen S, Fistarol GO, Granéli E (2005) Effects of cyanobacterial allelochemicals on a natural plankton community. Mar Ecol Prog Ser 287:1–9
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
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
Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge
Wrona FJ, Prowse TD, Reist JD et al (2006) Climate change effects on aquatic biota, ecosystem structure and function. AMBIO 35:359–369
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
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
Corresponding author
Additional information
Communicated by S. Dupont.
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-012-2078-3