Abstract
In Lake Tovel, an oligotrophic and weakly stratified lake, the dinoflagellate Borghiella dodgei Moestrup, Hansen et Daugbjerg, showed a peculiar spatial–temporal pattern with highest abundances in the bottom of the shallow side bay (4 m) along with remarkable abundance variations from year to year. We investigated B. dodgei’s growth in laboratory cultures and related results to their implication for bloom formation. B. dodgei was cultivated under different temperature, nutrient and light conditions. Growth rates, cell biovolume, cyst formation and pigment and mycosporine-like amino acids (MAAs) concentrations were determined. Experiments showed that this alga (i) had higher growth rates at low temperatures (<7°C) and high irradiance levels (~250 μmol m−2 s−1), (ii) produced higher yields with organic supplements such as peptone, (iii) did not grow in the dark even with organic supplements, (iv) survived for long periods without a light source, (v) synthesised MAAs, (vi) showed an increase in cell volume with nutrient shortage and increasing temperatures (>7°C) and (vii) had high encystment rates with temperatures >7°C. These laboratory fingerprints allowed us to construct a theoretical model defining the species’ niche. Borghiella needed a mixture of low temperatures, high irradiance levels and sufficient quantities of dissolved organic nitrogen to form blooms. Such a strict combination was probably a transient situation and occurred in oligotrophic Lake Tovel only in early summers followed by heavy spring rains.
Similar content being viewed by others
References
Alster, A., Z. Dubinsky & T. Zohary, 2006. Encystment of Peridinium gatunense: occurrence, favourable environmental conditions and its role in the dinoflagellate life cycle in a subtropical lake. Freshwater Biology 51: 1219–1228.
Andersen, R. A., S. L. Morton & J. P. Sexton, 1997. Provasoli-Guillard National Center for culture of marine phytoplankton, 1997 list of strains. Journal of Phycology 33(Suppl): 1–7.
Arrighetti, A. & M. Siligardi, 1978. Hydrobiological analyses from Lake Tovel, Trentino. Esperienze & Richerche 5: 5–69 (in Italian).
Boëchat, I. G., G. Weithoff, A. Krüger, B. Gücker & R. Adrian, 2007. A biochemical explanation for the success of mixotrophy in the flagellate Ochromonas sp. Limnology and Oceanography 52: 1624–1632.
Burford, M., 2005. Relative uptake of urea and ammonium by dinoflagellates or cyanobacterian shrimp mesocosms. Hydrobiologia 549: 297–303.
Butterwick, C., S. I. Heaney & J. F. Talling, 2005. Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshwater Biology 50: 291–300.
Calliari, D., M. Tolotti & F. Corradini, 2006. Littoral distribution of dinoflagellates in Lake Tovel (Trentino, Italy). Studi Trentini Scienze Naturali, Acta Biologica 81: 341–350.
Carli, L., P. Ferrari, O. Ferretti & G. B. Toller, 1981. Survey of the orographic horizon for the calculation of radiation and insolation in ten meteorological observatories. Esperienze & Ricerche 10: 107–154 (in Italian).
Chapman, A. D. & L. A. Pfiester, 1995. The effects of temperature, irradiance, and nitrogen on the encystment and growth of the fresh-water dinoflagellates Peridinium cinctum and P. willei in culture (Dinophyceae). Journal of Phycology 31: 355–359.
Coats, D. W., 2002. Dinoflagellate life-cycle complexities. Journal of Phycology 38: 417–419.
Corradini, F. & A. Boscaini, 2006. Physical and chemical characteristics of Lake Tovel (central Alps). Studi Trentini Scienze Naturali, Acta Biologica 81: 307–326 (in Italian).
Dixon, G. K. & P. J. Syrett, 1988. The growth of dinoflagellates in laboratory cultures. New Phytologist 109: 297–302.
Dodge, J. D., P. Mariani, A. Paganelli & R. Trevisan, 1987. Fine structure of the red-bloom dinoflagellate Glenodinium sanguineum, from Lake Tovel (N. Italy). Archiv für Hydrobiologie 78(Suppl): 125–138 (Algological Studies 47).
Droop, M. R., 1975. The nutrient status of algal cells in batch culture. Journal of the Marine Biological Association UK 55: 541–555.
Figueroa, R. I., I. Bravo & E. Garcés, 2006. Multiple routes of sexuality in Alexandrium taylori (Dinophyceae) in culture. Journal of Phycology 42: 1028–1039.
Filippi, M., G. Flaim, L. Ress, C. Salamon & M. Scotoni, 2006. A thermal gradient apparatus for algal growth experiments. Studi Trentini Scienze Naturali, Acta Biologica 81: 467–468.
Flaim, G., G. Hansen, Ø. Moestrup, F. Corradini & B. Borghi, 2004. Re-interpretation of the dinoflagellate ‘Glenodinium sanguineum’ in the reddening of Lake Tovel, Italian Alps. Phycologia 43: 737–743.
Frassanito, R., M. Cantonati, M. Tardio, I. Mancini & G. Guella, 2005. On-line identification of secondary metabolites in freshwater microalgae and cyanobacteria by combined liquid chromatography-photodiode array detection-mass spectrometric techniques. Journal of Chromatography A 1082: 33–42.
Freshfield, D. W., 1875. Italian Alps: Sketches in the Mountains of Ticino, Lombardy, the Trentino and Venetia. Longmans Green, London: 385.
Furusato, E. & T. Asaeda, 2009. A dynamic model of darkness tolerance for phytoplankton: model description. Hydrobiologia 619: 67–88.
Grigorszky, I., K. T. Kiss, V. Béres, I. Bácsi, M. M.- Hamvas, C. Máthé, G. Vasas, J. Padisák, G. Borics, M. Gligora & G. Borbély, 2006. The effects of temperature, nitrogen, and phosphorus on the encystment of Peridinium cinctum, Stein (Dinophyta). Hydrobiologia 563: 527–535.
Guillard, R. R., 1973. Division rates. In Stein, J. (ed.), Handbook of Phycological Methods. Cambridge University Press, Cambridge: 289–312.
Hansen, G. & G. Flaim, 2007. Dinoflagellates of the Trentino Province, Italy. Journal of Limnology 66: 107–141.
Hansen, G., N. Daugbjerg & P. Henriksen, 2007. Baldinia anauniensis gen. et sp. nov.: a ‘new’ dinoflagellate from Lake Tovel, N. Italy. Phycologia 46: 86–108.
Jensen, M. O. & Ø. Moestrup, 1997. Autecology of the toxic dinoflagellate Alexandrium ostenfeldii: life history and growth at different temperatures and salinities. European Journal of Phycology 32: 9–18.
John, E. H. & K. J. Flynn, 1999. Growth dynamics and toxicity of Alexandrium fundyense (Dinophyceae): the effect of changing N:P supply ratios on internal toxin and nutrient levels. European Journal of Phycology 35: 11–23.
Kilham, P., S. Kilham & R. E. Hecky, 1986. Hypothesized resource relationships among African planktonic diatoms. Limnology and Oceanography 31: 1169–1181.
Kremp, A., M. Elbrächter, M. Schweikert, J. Wolny & M. Gottschling, 2005. Woloszynskia halophila (Biecheler) comb.nov.: A bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. Journal of Phycology 41: 629–642.
Latasa, M. & E. Berdalet, 1994. Effect of nitrogen or phosphorus starvation on pigment composition of cultured Heterocapsa sp. Journal of Plankton Research 16: 83–94.
Laurion, I., A. Lami & R. Sommaruga, 2002. Distribution of mycosporine-like amino acids and photoprotective carotenoids among freshwater phytoplankton assemblages. Aquatic Microbial Ecology 26: 283–294.
Lindström, K., 1991. Nutrient requirements of the dinoflagellate Peridinium gatunense. Journal of Phycology 27: 207–219.
Litchman, E., P. J. Neale & A. T. Banaszak, 2002. Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: Photoprotection and repair. Limnology and Oceanography 47: 86–94.
Litaker, R. W., M. W. Vandersea, S. R. Kibler, V. J. Madden, E. J. Noga & P. A. Tester, 2002. Life cycle of the heterotrophic dinoflagellate Pfiesteria piscicida. Journal of Phycology 38: 442–463.
Louda, J. W., L. Liu & E. A. Baker, 2002. Senescence- and death-related alteration of chlorophylls and carotenoids in marine phytoplankton. Organic Geochemistry 33: 1635–1653.
Miller, W.E., J.C. Greene & T. Shiroyama, 1978. The Selenastrum capricornutum Printz algal assay bottle test. EPA -600/9-78-018.
Moestrup, Ø., G. Hansen, N. Daugbjerg, G. Flaim & M. D’Andrea, 2006. Studies on woloszynskioid dinoflagellates II: on Tovellia sanguinea sp. nov., the dinoflagellate responsible for reddening of Lake Tovel, Italy. European Journal of Phycology 41: 47–65.
Moestrup, Ø., G. Hansen & N. Daugbjerg, 2008. Studies on woloszynskioid dinoflagellates III: On Borghiella gen. nov., and B. dodgei sp. nov., a cold-water species from Lago di Tovel, N. Italy, and on B. tenuissima comb. nov. (syn. Woloszynskia tenuissima). Phycologia 47: 54–78.
Neale, P. J., A. T. Banaszak & C. R. Jarriel, 1998. Ultraviolet sunscreens in Gymnodinium sanguineaum (Dinophyceae): mycosporine-like amino acids protect against inhibition of photosynthesis. Journal of Phycology 34: 928–938.
Obertegger, U., G. Flaim, M. G. Braioni, R. Sommaruga, F. Corradini & A. Borsato, 2007. Water residence time as a driving force of zooplankton structure and succession. Aquatic Science 69: 575–583.
Obertegger, U., G. Flaim & R. Sommaruga, 2008. Multifactorial nature of rotifer water layer preferences in an oligotrophic lake. Journal of Plankton Research 30: 63–643.
Olli, K. & D. M. Anderson, 2002. High encystment success of the dinoflagellate Scrippsiella cf. lachrymose in culture experiments. Journal of Phycology 38: 145–156.
Pipp, E. & E. Rott, 1995. A phytoplankton compartment model for a small meromictic lake with special reference to species-specific niches and long-term changes. Ecological Modelling 78: 129–148.
Qiang, Hu, 2004. Environmental effects on cell composition. In Richmond, A. (ed.), Handbook of Microalgal Culture: Biotechnology and Applied Phycology. Blackwell Publishing Ltd, London: 83–94.
Raven, J. A. & R. J. Geider, 1988. Temperature and algal growth. New Phytologist 110: 441–461.
Rengefors, K., I. Karlsson & L. A. Hansson, 1998. Algal cyst dormancy: a temporal escape from herbivory. Proceedings Royal Society London B 265: 1353–1358.
Richardson, T. L., C. E. Gibson & S. I. Heaney, 2000. Temperature, growth and seasonal succession of phytoplankton in Lake Baikal, Siberia. Freshwater Biology 44: 431–440.
Rose, J. M. & D. A. Caron, 2007. Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters. Limnology and Oceanography 52: 886–895.
Rott, E., 1981. Some results from phytoplankton counting intercalibration. Schweizerische Zeitschrift für Hydrologie 43: 34–63.
Schmidtke, A., E. M. Bell & G. Weithoff, 2006. Potential grazing impact of the mixotrophic flagellate Ochromonas sp. (Chrysophyceae) on bacteria in an extremely acidic lake. Journal of Plankton Research 28: 991–1001.
Seaburg, K. G., B. C. Parker, R. A. Wharton & G. M. Simmons, 1981. Temperature-growth responses of algal isolates from Antarctic oases. Journal of Phycology 17: 353–360.
Sgrosso, S., F. Esposito & M. Montresor, 2001. Temperature and daylength regulate encystment in calcareous cyst-forming dinoflagellates. Marine Ecology Progress Series 211: 77–87.
Sigee, D. C., F. Bahrami, B. Estrada, R. E. Webster & A. P. Dean, 2007. The influence of phosphorus availability on carbon allocation and P quota in Scenedesmus subspicatus: a synchrotrom-based FTIR analysis. Phycologia 46: 583–592.
Skovgaard, A., 2000. A phagotrophically derivable growth factor in the plastidic dinoflagellate Gyrodinium resplendens (Dinophyceae). Journal of Phycology 36: 1069–1078.
Smayda, T., 2002. Adaptive ecology, growth strategies and the global bloom expansion of dinoflagellates. Journal of Oceanography 58: 281–294.
Sommaruga, R., 2001. The role of solar UV radiation in the ecology of alpine lakes. Journal of Photochemistry and Photobiology B: Biology 62: 35–42.
Staehr, P. A. & M. J. Birkeland, 2006. Temperature acclimation of growth, photosynthesis and respiration in two mesophilic phytoplankton species. Phycologia 45: 648–656.
Tang, E., 1996. Why do dinoflagellates have lower growth rates? Journal of Phycology 32: 80–84.
Thingstad, T. F., L. Ovreas, J. K. Egge, T. Lovdal & M. Heldal, 2005. Use of non-limiting substrates to increase size, a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs? Ecology Letters 8: 65–682.
Tolotti, M., D. Calliari & F. Corradini, 2006. Interannual variability of phytoplankton in Lake Tovel (central Alps). Studi Trentini Scienze Naturali, Acta Biologica 81: 327–340 (in Italian).
van de Poll, W. H., M. A. van Leeuwe, J. Roggeveld & A. G. J. Buma, 2005. Nutrient limitation and high irradiance acclimation reduce PAR and UV induced viability loss in the Antarctic diatom Chaetoceros brevis. Journal of Phycology 41: 840–850.
Whitehead, K. & J. I. Hedges, 2002. Analysis of mycosporine-like amino acids in plankton by liquid chromatography electrospray ionization mass spectrometry. Marine Chemistry 80: 27–39.
Acknowledgements
This study was presented as a contributed article at the Bat Sheva de Rothschild seminar on Phytoplankton in the Physical Environment—the fifteenth workshop of the International Association of phytoplankton taxonomy and ecology (IAP). GF thanks Ø. Moestrup (Uni. Copenhagen—DK) for generously providing the Borghiella culture and introducing her to the world of dinoflagellates. The authors also thank R. Sommaruga (Uni. Innsbruck—A) for UVR measurements, D. Tait for DOC analyses, F. Corradini for chemical analyses, F. Ciutti and A. Gandolfi for comments, V. Pinamonti and G. Leonardi for sampling, L. Ress, D. Calliari and L. Dal Bello for cell counts. This study was partially funded by the research project ECOPLAN (Province of Trento, Italy).
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is dedicated to Univ. Prof. Mag. Dr. Walter Larcher (Institute of Botany, University of Innsbruck), a leading pioneer in eco-physiological research of plants, on the occasion of his 80th birthday
Guest editors: T. Zohary, J. Padisák & L. Naselli-Flores / Phytoplankton in the Physical Environment: Articles from the 15th Workshop of the International Association for Phytoplankton Taxonomy and Ecology (IAP), held at the Ramot Holiday Resort on the Golan Heights, Israel, 23–30 November 2008
Rights and permissions
About this article
Cite this article
Flaim, G., Rott, E., Frassanito, R. et al. Eco-fingerprinting of the dinoflagellate Borghiella dodgei: experimental evidence of a specific environmental niche. Hydrobiologia 639, 85–98 (2010). https://doi.org/10.1007/s10750-009-0013-5
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-009-0013-5