Abstract
Thermal stratification is increasing in strength as a result of higher surface water temperature. This could influence the vertical distribution of vertically migrating dinoflagellates. We studied the diel vertical distribution of the dinoflagellates Heterocapsa triquetra and Prorocentrum minimum using stratified laboratory columns with two thermoclines of different strength (ΔT° = 10 or 17 °C), with below cline temperature of 8 °C. Above the thermocline, nutrient depletion simulated the natural summer conditions in the Baltic Sea. Our study shows that H. triquetra and P. minimum can behave differently in terms of their vertical occurrence, both in space and in time when subjected to thermoclines of different strength. Also, both dinoflagellate species showed species-specific distribution patterns. In the ΔT° = 10 °C treatment, H. triquetra cells performed a diel vertical migration (DVM) behavior just above the thermocline, but not in the ΔT° = 17 °C. In the ΔT° = 17 °C, the cells did not migrate and cell densities in the water column decreased over time. Opposing results were observed for P. minimum, where a DVM pattern was found exclusively below the thermocline of ΔT° = 17 °C, while in the ΔT° = 10 °C treatment, no clear DVM pattern was observed, and the highest number of cells were found in the cold bottom water. These results indicate that an increase in thermal stratification can influence species-specific dinoflagellate distribution, behavior, and survival.
Similar content being viewed by others
References
Baek SH, Ki JS, Katano T, You K, Park BS, Shin HH, Shin K, Kim YO, Han M-S (2011) Dense winter bloom of the dinoflagellate Heterocapsa triquetra below the thick surface ice of brackish Lake Shihwa, Korea. Phycol Res 59:273–285
Behrenfeld JM, Worthington K, Sherrell MR, Chavez PF, Strutton P, McPhaden M, Shea MD (2006) Controls on tropical Pacific productivity revealed through nutrient stress diagnostics. Nature 442:1025–1028
Bollens SM, Rollwagen-Bollens G, Quenette JA, Bochdansky B (2011) Cascading migrations and implications for vertical fluxes in pelagic ecosystems. J Plankton Res 33:349–355
Bollens SM, Quenette JA, Rollwagen-Bollens G (2012) Predator-enhanced diel vertical migration in a planktonic dinoflagellate. Mar Ecol Prog Ser 447:49–54
Coma R, Ribes M, Serrana E, Jim’enez E, Salat J, Pascual J (2009) Global warming-enhanced stratification and mass mortality events in the Mediterranean. PNAS 106:6176–6181
Dale B, Edwards M, Reid PC (2006) Climate change and harmful algal blooms. In: Granéli E, Turner JT (eds) Ecology of harmful algae. Springer, Berlin Heidelberg, pp 367–378
Doney SC (2006) Plankton in a warmer world. Nature 444:69–696
Garce´s E (2002) Temporary cysts in dinoflagellates. In: Garce´s E, Zingone A, Montresor M, Reguera B, Dale B (eds) LIFEHAB: life histories of microalgal species causing harmful algal blooms. European Commission, Luxembourg, pp 46–48
Grzebyk G, Berland B (1996) Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from the Mediterranean Sea. J Plankton Res 18:1837–1849
Guillard RLL, Ryther JH (1962) Studies of marine planktonic diatoms: in Cyclotella nana Hustedt and Detonula confervacea (Cleve). Gran Can J Microbiol 8:229–239
Hajdu S, Pertola S, Kuosa H (2005) Prorocentrum minimum (Dinophyceae) in the Baltic Sea: morphology, occurrence-a review. Harmful Algae 4:471–480
Hällfors H, Hajdu S, Kuosa H, Larsson U (2011) Vertical and temporal distribution of the dinoflagellates Dinophysis acuminata and D. norvegica in the Baltic Sea. Boreal Environ Res 16:121–135
Hällfors H, Backer H, Leppanen JM, Hällfors S, Hällfors G, Kuosa H (2013) The northern Baltic Sea phytoplankton communities in 1903–1911 and 1993–2005: a comparison of historical and modern species data. Hydrobiologia 707:109–133
Hansen PJ (1995) Growth and grazing response of a ciliate feeding on the red tide dinoflagellate Gyrodinium aureolum in monoculture and in mixture with a non-toxic alga. Mar Ecol Prog Ser 121:65–72
Hardeland R (1994) Induction of cyst formation by low temperature. Experientia 50:60–62
Heaney SI, Eppley RW (1981) Light, temperature and nitrogen as interacting factors affecting diel vertical migration of dinoflagellates in culture. J Plankton Res 3:331–344
Heaney SI, Furnass TI (1980) Laboratory models of diel migration of the dinoflagellate Ceratium hirundinella. Freshw Biol 10:163–170
HELCOM (2007) Climate change in the Baltic Sea area HELCOM Thematic Assessment in 2007 Baltic Sea Environment. Proceedings No 111
Intergovernmental Panel on Climate Change (IPCC) (2007) Coastal systems and low-lying areas climate change: impacts, adaptation and vulnerability contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change. In: Parry ML, Canziani OF, Palutikof JP, Van der Linden PJ, Hanson CE (eds) Coastal systems and low-lying areas. Cambridge Univ Press Cambridge, UK, pp 315–356
Jensen MO, Moestrup O (1997) Autoecology of the toxic dinoflagellate Alexandrium ostenfeldii: life history and growth at different temperatures and salinities. Eur J Phyc 32:9–18
Jephson T, Carlsson P (2009) Species-and stratification-dependent diel vertical migration behaviour of three dinoflagellate species in a laboratory study. J Plankton Res 31:1353–1362
Jephson T, Fagerberg T, Carlsson P (2011) Dependency of dinoflagellate vertical migration on salinity stratification. Aquat Microb Ecol 63:255–264
Kamykowski D (1981) Laboratory experiments on the diurnal vertical migration on marine dinoflagellates through temperature gradients. Mar Biol 62:57–64
Kamykowski D, McCollum AS (1986) The temperature acclimatized swimming rate of selected marine dinoflagellates. J Plankton Res 8:275–287
Kamykowski D, Zentara SJ (1977) The diurnal vertical migration of the motile phytoplankton through temperature gradients. Limnol Oceanogr 22:148–152
Kamykowski D, Milligan E, Reed RE (1998) Biochemical relationships with the orientation of the autotrophic dinoflagellate Gymnodinium breve under nutrient replete conditions. Mar Ecol Prog Ser 167:105–117
Kimura T, Watanabe M, Kohata K, Sudo R (1999) Phosphate metabolism during diel vertical migration in the raphidophycean alga, Chattonella antique. J Appl Phycol 11:301–311
Kononen K, Huttunen M, Hällfors S, Gentien P, Lunven M, Huttula T, Laanemets J, Lilover M, Pavelson J, Stips A (2003) Development of a deep chlorophyll maximum of Heterocapsa triquetra Eherenb at the entrance to the Gulf of Finland. Limnol Oceanogr 48:594–607
Laanemets J, Kononen K, Pavelson J, Poutanen EL (2004) Vertical location of seasonal nutriclines in the western Gulf of Finland. J Mar Syst 52:1–13
Levandowsky M, Kaneta PJ (1987) Behavior in dinoflagellates. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell, Oxford, pp 360–398
Levitus S, Antonov J, Boyer T (2005) Warming of the world ocean, 1955–2003. Geophys Res Lett 32:L02604
Lindholm T, Nummelin C (1999) Red tide of the dinoflagellate Heterocapsa triquetra (Dinophyta) in ferry-mixed coastal inlet. Hydrobiologia 393:245–251
Lips U, Lips I, Liblik T, Kuvaldina N (2010) Processes responsible for the formation and maintenance of sub-surface chlorophyll maxima in the Gulf of Finland. Estuar Coast Shelf Sci 88:339–349
Litaker RW, Warner VE, Rhyne C, Duke CS, Kenney BE, Ramus J, Tester PA (2002) Effect of diel and interday variations in light on the cell division pattern and in situ growth rates of the bloom-forming dinoflagellates Heterocapsa triquetra. Mar Ecol Prog Ser 232:63–74
MacIntyre JG, Cullen JJ, Cembella AD (1997) Vertical migration, nutrition and toxicity in the dinoflagellates Alexandrium tamarense. Mar Ecol Prog Ser 148:201–216
Nielsen LT, Lundholm N, Hansen PJ (2007) Does irradiance influence the tolerance of marine phytoplankton to high pH? Mar Biol Res 3:446–453
Olli K (2004) Temporary cyst formation of Heterocapsa triquetra (Dinophyceae) in natural populations. Mar Biol 145:1–8
Olsson P, Graneli E (1991) Observations on diurnal vertical migration and phased cell division for three coexisting marine dinoflagellates. J Plankton Res 13:1313–1324
Richardson K, Beardall J, Raven JA (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol 93:157–191
Richter PR, Hader DP, Goncalves RJ et al (2007) Vertical migration and motility responses in three marine phytoplankton species exposed to solar radiation. Photochem Photobiol 83:810–817
Ross ON, Sharples J (2007) Phytoplankton motility and the competition for nutrients in the thermocline. Mar Ecol Prog Ser 347:21–38
Ruosteenoja K, Tuomenvirta H, Jylhä K (2007) GCM-based regional temperature and precipitation change estimates for Europe under four SRES scenarios applying super-ensemble pattern-scaling method. Clim Change 81:193–208
Schernewski G, Hofstede J, Neumann T (2011) Global change and Baltic coastal zones, vol 1. Springer, Dordrecht, p 1
Sherman K, Belkin IM, Friedland KD, O’Reilly J, Hyde K (2009) Accelerated warming and emergent trends in fisheries biomass yields of the world’s large marine ecosystems. Ambio 38:215–224
Sjöqvist C, Lindholm TJ (2011) Natural co-occurrence of Dinophysis acuminata (Dinoflagellata) and Mesodinium rubrum (Ciliophora) in thin layers in a coastal inlet. J Eukaryot Microbiol 58:365–372
Smayda TJ, Reynolds CS (2001) Community assembly in marine phytoplankton: application of recent models to harmful dinoflagellate blooms. J Plankton Res 23:447–461
Tangen K (1980) Brown water in the Oslofjord, Norway, in September 1979 caused by the toxic Prorocentrum minimum and other dinoflagellates. Blyttia 38:145–155
Throndsen J (1973) Motility in some marine nanoplankton flagellates. Norw J Zool 21:193–200
Valderrama JC (1995) Methods of nutrient analysis. In: Hallegraeff GM, Anderson DM, Cembella AD (eds) Manual of harmful marine microalgae. IOC Manual No 33. UNESCO, Paris, pp 252–268
Venrick EL (1978) How many cells to count? In: Sournia A (ed) Phytoplankton manual UNESCO. Page Brothers, Norwich, pp 167–180
Wong KTM, Lee JHW, Hodgkiss IJ (2007) A simple model for forecast of coastal algal blooms. Estuar Coast Shelf Sci 74:175–196
Yamazaki H, Kamykowski D (1991) The vertical trajectories of motile phytoplankton in a wind-mixed water column. Deep Sea Res 38:219–241
Acknowledgments
We thank Monica Appelgren (University of Gothenburg Marine Culture—GUMACC), University of Gothenburg, Department of Biological and Environmental Sciences, for supplying the dinoflagellate cultures. We also thank the Royal Swedish Academy of Sciences and the Carl Trygger foundation for funding this project.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by U.-G. Berninger.
Rights and permissions
About this article
Cite this article
de Souza, K.B., Jephson, T., Hasper, T.B. et al. Species-specific dinoflagellate vertical distribution in temperature-stratified waters. Mar Biol 161, 1725–1734 (2014). https://doi.org/10.1007/s00227-014-2446-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-014-2446-2