Marine Biology

, Volume 161, Issue 8, pp 1725–1734 | Cite as

Species-specific dinoflagellate vertical distribution in temperature-stratified waters

  • Karine Bresolin de Souza
  • Therese JephsonEmail author
  • Thomas Berg Hasper
  • Per Carlsson
Original Paper


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.


Dinoflagellate Bottom Water Diel Vertical Migration Deep Chlorophyll Maximum Dinoflagellate Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



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.


  1. 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 59:273–285CrossRefGoogle Scholar
  2. 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 442:1025–1028CrossRefGoogle Scholar
  3. Bollens SM, Rollwagen-Bollens G, Quenette JA, Bochdansky B (2011) Cascading migrations and implications for vertical fluxes in pelagic ecosystems. J Plankton Res 33:349–355CrossRefGoogle Scholar
  4. Bollens SM, Quenette JA, Rollwagen-Bollens G (2012) Predator-enhanced diel vertical migration in a planktonic dinoflagellate. Mar Ecol Prog Ser 447:49–54CrossRefGoogle Scholar
  5. 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 106:6176–6181CrossRefGoogle Scholar
  6. 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 367–378CrossRefGoogle Scholar
  7. Doney SC (2006) Plankton in a warmer world. Nature 444:69–696CrossRefGoogle Scholar
  8. 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 46–48Google Scholar
  9. Grzebyk G, Berland B (1996) Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from the Mediterranean Sea. J Plankton Res 18:1837–1849CrossRefGoogle Scholar
  10. Guillard RLL, Ryther JH (1962) Studies of marine planktonic diatoms: in Cyclotella nana Hustedt and Detonula confervacea (Cleve). Gran Can J Microbiol 8:229–239CrossRefGoogle Scholar
  11. Hajdu S, Pertola S, Kuosa H (2005) Prorocentrum minimum (Dinophyceae) in the Baltic Sea: morphology, occurrence-a review. Harmful Algae 4:471–480CrossRefGoogle Scholar
  12. 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 16:121–135Google Scholar
  13. 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 707:109–133CrossRefGoogle Scholar
  14. 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 121:65–72CrossRefGoogle Scholar
  15. Hardeland R (1994) Induction of cyst formation by low temperature. Experientia 50:60–62CrossRefGoogle Scholar
  16. Heaney SI, Eppley RW (1981) Light, temperature and nitrogen as interacting factors affecting diel vertical migration of dinoflagellates in culture. J Plankton Res 3:331–344CrossRefGoogle Scholar
  17. Heaney SI, Furnass TI (1980) Laboratory models of diel migration of the dinoflagellate Ceratium hirundinella. Freshw Biol 10:163–170CrossRefGoogle Scholar
  18. HELCOM (2007) Climate change in the Baltic Sea area HELCOM Thematic Assessment in 2007 Baltic Sea Environment. Proceedings No 111Google Scholar
  19. 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 315–356Google Scholar
  20. Jensen MO, Moestrup O (1997) Autoecology of the toxic dinoflagellate Alexandrium ostenfeldii: life history and growth at different temperatures and salinities. Eur J Phyc 32:9–18CrossRefGoogle Scholar
  21. Jephson T, Carlsson P (2009) Species-and stratification-dependent diel vertical migration behaviour of three dinoflagellate species in a laboratory study. J Plankton Res 31:1353–1362CrossRefGoogle Scholar
  22. Jephson T, Fagerberg T, Carlsson P (2011) Dependency of dinoflagellate vertical migration on salinity stratification. Aquat Microb Ecol 63:255–264CrossRefGoogle Scholar
  23. Kamykowski D (1981) Laboratory experiments on the diurnal vertical migration on marine dinoflagellates through temperature gradients. Mar Biol 62:57–64CrossRefGoogle Scholar
  24. Kamykowski D, McCollum AS (1986) The temperature acclimatized swimming rate of selected marine dinoflagellates. J Plankton Res 8:275–287CrossRefGoogle Scholar
  25. Kamykowski D, Zentara SJ (1977) The diurnal vertical migration of the motile phytoplankton through temperature gradients. Limnol Oceanogr 22:148–152CrossRefGoogle Scholar
  26. 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 167:105–117CrossRefGoogle Scholar
  27. Kimura T, Watanabe M, Kohata K, Sudo R (1999) Phosphate metabolism during diel vertical migration in the raphidophycean alga, Chattonella antique. J Appl Phycol 11:301–311CrossRefGoogle Scholar
  28. 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 48:594–607CrossRefGoogle Scholar
  29. Laanemets J, Kononen K, Pavelson J, Poutanen EL (2004) Vertical location of seasonal nutriclines in the western Gulf of Finland. J Mar Syst 52:1–13CrossRefGoogle Scholar
  30. Levandowsky M, Kaneta PJ (1987) Behavior in dinoflagellates. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell, Oxford, pp 360–398Google Scholar
  31. Levitus S, Antonov J, Boyer T (2005) Warming of the world ocean, 1955–2003. Geophys Res Lett 32:L02604Google Scholar
  32. Lindholm T, Nummelin C (1999) Red tide of the dinoflagellate Heterocapsa triquetra (Dinophyta) in ferry-mixed coastal inlet. Hydrobiologia 393:245–251CrossRefGoogle Scholar
  33. 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 88:339–349CrossRefGoogle Scholar
  34. 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 232:63–74CrossRefGoogle Scholar
  35. MacIntyre JG, Cullen JJ, Cembella AD (1997) Vertical migration, nutrition and toxicity in the dinoflagellates Alexandrium tamarense. Mar Ecol Prog Ser 148:201–216CrossRefGoogle Scholar
  36. Nielsen LT, Lundholm N, Hansen PJ (2007) Does irradiance influence the tolerance of marine phytoplankton to high pH? Mar Biol Res 3:446–453CrossRefGoogle Scholar
  37. Olli K (2004) Temporary cyst formation of Heterocapsa triquetra (Dinophyceae) in natural populations. Mar Biol 145:1–8CrossRefGoogle Scholar
  38. Olsson P, Graneli E (1991) Observations on diurnal vertical migration and phased cell division for three coexisting marine dinoflagellates. J Plankton Res 13:1313–1324CrossRefGoogle Scholar
  39. Richardson K, Beardall J, Raven JA (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol 93:157–191CrossRefGoogle Scholar
  40. 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 83:810–817CrossRefGoogle Scholar
  41. Ross ON, Sharples J (2007) Phytoplankton motility and the competition for nutrients in the thermocline. Mar Ecol Prog Ser 347:21–38CrossRefGoogle Scholar
  42. 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 81:193–208CrossRefGoogle Scholar
  43. Schernewski G, Hofstede J, Neumann T (2011) Global change and Baltic coastal zones, vol 1. Springer, Dordrecht, p 1Google Scholar
  44. 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 38:215–224CrossRefGoogle Scholar
  45. 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 58:365–372CrossRefGoogle Scholar
  46. Smayda TJ, Reynolds CS (2001) Community assembly in marine phytoplankton: application of recent models to harmful dinoflagellate blooms. J Plankton Res 23:447–461CrossRefGoogle Scholar
  47. Tangen K (1980) Brown water in the Oslofjord, Norway, in September 1979 caused by the toxic Prorocentrum minimum and other dinoflagellates. Blyttia 38:145–155Google Scholar
  48. Throndsen J (1973) Motility in some marine nanoplankton flagellates. Norw J Zool 21:193–200Google Scholar
  49. 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 252–268Google Scholar
  50. Venrick EL (1978) How many cells to count? In: Sournia A (ed) Phytoplankton manual UNESCO. Page Brothers, Norwich, pp 167–180Google Scholar
  51. Wong KTM, Lee JHW, Hodgkiss IJ (2007) A simple model for forecast of coastal algal blooms. Estuar Coast Shelf Sci 74:175–196CrossRefGoogle Scholar
  52. Yamazaki H, Kamykowski D (1991) The vertical trajectories of motile phytoplankton in a wind-mixed water column. Deep Sea Res 38:219–241CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Karine Bresolin de Souza
    • 1
  • Therese Jephson
    • 2
    Email author
  • Thomas Berg Hasper
    • 1
  • Per Carlsson
    • 2
  1. 1.Department of Biological and Environmental SciencesUniversity of GothenburgGothenburgSweden
  2. 2.Department of Biology, Aquatic EcologyLund UniversityLundSweden

Personalised recommendations