Skip to main content

Advertisement

Log in

Temporary cyst formation of Heterocapsa triquetra (Dinophyceae) in natural populations

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Heterocapsa triquetra (Ehrenberg) Stein is a phototrophic marine dinoflagellate with wide coastal distribution. It is known to be capable of mixotrophy and diel vertical migration. The species was particularly abundant in the Gulf of Finland (the Baltic Sea) during the summers of 1996 and 1998, leading to discolouration of water on the south-west coast of Finland. Large-scale (50 m3) coastal mesocosm experiments in the north-west Gulf of Finland (the Baltic Sea) in the summers of 1996 and 1998 with daily mineral nutrient additions provoked a biomass increase of phytoplankton dominated by H. triquetra. From the first days of the experiment temporary cysts of H. triquetra were found in the bottom sediment water of the mesocosms. Maximum temporary cyst production rates reached values up to 20×106 cysts m−2 day−1, accounting for <1% of the depth-integrated motile population size. The environmental features favouring temporary cyst production remain uncertain; zooplankton grazing and nutrient stress are potential factors. Temporary cysts of H. triquetra were observed in a unialgal culture (f/2 medium) isolated in summer 1999 from Eel Pond (Woods Hole, Mass., USA).

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3a–c
Fig. 4a-e
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aelion CM, Chisholm SW (1985) Effect of temperature on growth and ingestion rates of Flavella sp. J Plankton Res 7:821–830

    Google Scholar 

  • Anderson DM, Lindquist NL (1985) Time-course measurements of phosphorus depletion and cyst formation in the dinoflagellate Gonyaulax tamarensis Lebour. J Exp Mar Biol Ecol 86:1–13

    Article  Google Scholar 

  • Anderson DM, Stolzenbach KD (1985) Selective retention of two dinoflagellates in a well-mixed estuarine embayment: the importance of diel vertical migration and surface avoidance. Mar Ecol Prog Ser 25:39–50

    Google Scholar 

  • Anderson DM, Wall D (1978) Potential importance of benthic cysts of Gonyaulax tamarensis and Gonyaulax excavata in initiating toxic dinoflagellate blooms. J Phycol 14:224–234

    Google Scholar 

  • Anderson DM, Coats DW, Tyler MA (1985) Encystment of the dinoflagellate Gyrodinium uncatenum: temperature and nutrient effects. J Phycol 21:200–206

    Google Scholar 

  • Balzer I, Hardeland R (1992) Effects of indoleamines and short photoperiods on the encystment of Gonyaulax polyedra. Chronobiol Int 9:260–265

    CAS  PubMed  Google Scholar 

  • Braarud T, Pappas I (1951) Experimental studies on the dinoflagellate Peridinium triquetrum (Ehrb.) Lebour. Avh Norsk Vidensk Akad Oslo I Mat-Naturv 2:2–22

  • Coats DW, Tyler MA, Anderson DM (1984) Sexual processes in the life cycle of Gyrodinium uncatenatum (Dinophyceae): a morphogenetic overview. J Phycol 20:351–361

    Google Scholar 

  • Garcés E (2002) Temporary cysts in dinoflagellates. In: Garcés 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

  • Garcés E, Delgado M, Masó M, Camp J (1998) Life history and in situ growth rates of Alexandrium taylori (Dinophyceae, Pyrrophyta). J Phycol 34:880–887

    Article  Google Scholar 

  • Garcés E, Masó M, Camp J (1999) A recurrent and localized dinoflagellate bloom in a Mediterranean beach. J Plankton Res 21:2373–2391

    Article  Google Scholar 

  • Garcés E, Masó M, Camp J (2002) Role of temporary cysts in the population dynamics of Alexandrium taylori (Dinophyceae). J Plankton Res 24:681–686

    Article  Google Scholar 

  • Gifford DJ (1985) Laboratory culture of marine planktonic oligotrichs (Ciliophora, Oligotrichida). Mar Ecol Prog Ser 23:257–267

    Google Scholar 

  • Grzebyk D, Berland B (1996) Influence of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from the Mediterranean Sea. J Plankton Res 35:331–338

    Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms I. Cyclotella nana Hustedt and Detonula confervaceae (Cleve) Gran. Can J Microbiol 8:229–239

    CAS  Google Scholar 

  • Haapala J (1994) Upwelling and its influence on nutrient concentration in the coastal area of the Hanko peninsula, entrance of the Gulf of Finland. Estuar Coast Shelf Sci 38:507–521

    Article  CAS  Google Scholar 

  • 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 algae. Mar Ecol Prog Ser 121:65–72

    Google Scholar 

  • Hardeland R (1994) Induction of cyst formation by low temperature. Experientia 50:60–62

    Google Scholar 

  • Jensen MO, Moestrup Ø (1997) Autecology of the toxic dinoflagellate Alexandrium ostenfeldii: life history and growth at different temperatures and salinities. Eur J Phycol 32:9–18

    Article  Google Scholar 

  • Kamiyama T (1997) Growth and grazing responses of tintinnid ciliates feeding on the toxic dinoflagellate Heterocapsa circularisquama. Mar Biol 128:509–515

    Article  Google Scholar 

  • Kim H-G, Park J-S, Lee S-G (1990) Coastal algal blooms caused by the cyst-forming dinoflagellates. Bull Korean Fish Soc 23:468–474

    Google Scholar 

  • Kita T, Fukuyo Y, Tokuda H, Hirano R (1985) Life history and ecology of Gonyodoma pseudogonyaulax (Pyrrophyta) in a rockpool. Bull Mar Sci 37:643–651

    Google Scholar 

  • Kivi K, Kaitala S, Kuosa H, Kuparinen J, Leskinen E, Lignell R, Marcussen B, Tamminen T (1993) Nutrient limitation and grazing control of the Baltic plankton community during annual succession. Limnol Oceanogr 38:893–905

    Google Scholar 

  • Larsson U, Hajdu S, Andersson L, Edler E, Sundelin B, Eriksson AK (2001) Surface waters and phytoplankton. Östersjö ‘98:27–32

  • Legrand C, Granéli E, Carlsson P (1998) Induced phagotrophy in the photosynthetic dinoflagellate Heterocapsa triquetra. Aquat Microb Ecol 15:65–75

    Google Scholar 

  • Lindholm T, Nummelin C (1999) Red tide of the dinoflagellate Heterocapsa triquetra (Dinophyta) in a ferry-mixed coastal inlet. Hydrobiologia 393:245–251

    Article  CAS  Google Scholar 

  • Lindholm T, Öhman P (1995) Occurrence of bloom-forming and potentially harmful phytoplankton in the Åland archipelago in the summer of 1993. Memoranda Soc Fauna Flora Fenn 71:10–18

    Google Scholar 

  • Montresor M (2002) To what extent are dinoflagellate life histories important for HABs? In: Garcés E, Zingone A, Montresor M, Reguera B, Dale B (eds) LIFEHAB: life histories of microalgal species causing harmful algal blooms. European Commission, Luxembourg, pp 18–21

  • Nagasaki K, Yamaguchi M, Imai I (2000) Algicidal activity of a killer bacterium against the harmful red tide dinoflagellate Heterocapsa circularisquama isolated from Ago Bay, Japan. Bull Jpn Soc Sci Fish 66:666–673

    Google Scholar 

  • Nakamura Y, Suzuki S-V, Hiromi J (1995) Growth and grazing of a naked heterotrophic dinoflagellate, Gyrodinium dominans. Aquat Microb Ecol 9:157–164

    Google Scholar 

  • Naustvoll L-J (2000) Prey size spectra in naked heterotrophic dinoflagellates. Phycologia 39:448–455

    Google Scholar 

  • Niemi Å (1975) Ecology of phytoplankton in the Tvärminne area, SW coast of Finland II. Primary production and environmental conditions in the archipelago and the sea zone. Acta Bot Fenn 105:1–73

    Google Scholar 

  • Olli K (1996) Resting cyst formation of Eutreptiella gymnastica (Euglenophyceae) in the northern coastal Baltic Sea. J Phycol 32:535–542

    Google Scholar 

  • Olli K, Seppälä J (2001) Vertical niche separation of phytoplankton: large-scale mesocosm experiments. Mar Ecol Prog Ser 217:219–233

    Google Scholar 

  • Olli K, Heiskanen A-S, Seppälä J (1996) Development and fate of Eutreptialla gymnastica bloom in nutrient enriched enclosures in the coastal Baltic Sea. J Plankton Res 18:1587–1604

    Google Scholar 

  • Pfiester LA (1977) Sexual reproduction of Peridinium gatunense (Dinophyceae). J Phycol 13:92–95

    Google Scholar 

  • Pfiester LA, Anderson DM (1987) Dinoflagellate reproduction. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell Scientific, Oxford, pp 611–648

  • Rengefors K, Karlsson I, Hansson LA (1998) Algal cyst dormancy: a temporary escape from herbivory. Proc R Soc Lond B 265:1353–1358

    Article  Google Scholar 

  • Schmitter RE (1979) Temporary cysts of Gonyaulax excavata: effects of temperature and light. In: Taylor DL, Seliger HH (eds) Toxic dinoflagellate blooms. Elsevier, New York

  • Stoecker DK, Sanders NK (1985) Differential grazing by Acartia tonsa on a dinoflagellate and a tintinnid. Mar Ecol Prog Ser 7:85–100

    Google Scholar 

  • Tarutani K, Nagasaki K, Itakura S, Yamaguchi M (2001) Isolation of a virus infecting the novel shellfish-killing dinoflagellate Heterocapsa circularisquama. Aquat Microb Ecol 23:103–111

    Google Scholar 

  • Välikangas I (1926) Planktologische Untersuchungen im Hafengebiet von Helsingfors I. Über das Plankton insbesondere der Netz-zooplankton des Sommerhalbjahres. Acta Zool Fenn 1:1–298

    Google Scholar 

  • Walker LM (1984) Life histories, dispersal, and survival in marine planktonic dinoflagellates. In: Steidinger KA, Walker LM (eds) Marine plankton life cycle strategies. CRC Press, Boca Raton, Fla., pp 19–34

  • Xiao Y, Qi Y, Wang Z, Lu S (2001) The relationship between Scrippsiella trochoidea red tide and cysts in the Daya Bay. Mar Sci Haiyang Kexue 25:50–54

    Google Scholar 

Download references

Acknowledgements

This study was supported by the Estonian Science Foundation (ETF 3329, 5262), the European Commission through the FATE project (EC grant EVK3-2001-00050), the Walter and Andreé de Nottbeck Foundation, Fulbright Foundation, and NSF/NATO grant DGE-9804544. I am grateful to the research team PELAG (T. Tamminen, A.S. Heiskanen, R. Lignell, K. Kivi, P. Tuomi, and P. Kuuppo) for planning and executing the mesocosm experiments. Special thanks to the staff of the Tvärminne zoological station (University of Helsinki) for their help and hospitality. Critical remarks of the two anonymous reviewers are gratefully acknowledged. The mesocosm experiments were part of a MAST III project COMWEB (no. CT960052). This is contribution no. 11067 of the Woods Hole Oceanographic Institution.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. Olli.

Additional information

Communicated by M. Kühl, Helsingør

Rights and permissions

Reprints and permissions

About this article

Cite this article

Olli, K. Temporary cyst formation of Heterocapsa triquetra (Dinophyceae) in natural populations. Marine Biology 145, 1–8 (2004). https://doi.org/10.1007/s00227-004-1295-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-004-1295-9

Keywords

Navigation