The life cycle of many dinoflagellates includes at least one nonflagellated benthic stage (cyst). In the literature, the different types of dinoflagellate cysts are mainly defined based on morphological (number and type of layers in the cell wall) and functional (long- or short-term endurance) differences. These characteristics were initially thought to clearly distinguish pellicle (thin-walled) cysts from resting (double-walled) dinoflagellate cysts. The former were considered short-term (temporal) and the latter long-term (resting) cysts. However, during the last two decades further knowledge has highlighted the great intricacy of dinoflagellate life histories, the ecological significance of cyst stages, and the need to clarify the functional and morphological complexities of the different cyst types. Here we review and, when necessary, redefine the concepts of resting and pellicle cysts, examining both their structural and their functional characteristics in the context of the life cycle strategies of several dinoflagellate species.
References
[1]
Cavalier-Smith, T. Origins of the machinery of recombination and sex. Heredity 2002, 88, 125–141, doi:10.1038/sj.hdy.6800034.
[2]
Wagmann, K.; Hautekeete, N.; Piquot, Y.; Meunier, C.; Schmitt, S.; van Dijk, H. Seed dormancy distribution: Explanatory ecological factors. Ann. Bot. 2012, 110, 1205–1219, doi:10.1093/aob/mcs194.
[3]
Debieu, M.; Tang, C.; Stich, B.; Sikosek, T.; Effgen, S.; Josephs, E.; Schmitt, J.; Nordborg, M.; Koornneef, M.; de Meaux, J. Co-variation between seed dormancy, growth rate and flowering time changes with latitude in Arabidopsis thaliana. PLoS One 2013, 8, e61075.
[4]
Reinsch, P.F. Die palinosph?rien, ein mikroskopischer vegetabile organismus in der mukronatenkreide. Cent. Miner. Geol. Palaeontol. 1905, 402–407.
[5]
Erdtman, G. Fynd av Hystrichosphaera furcata i Gullmaren. Geologiska F?reningen I Stokholmen F?rhanlingar 1950, 72, 221, doi:10.1080/11035895009454146.
[6]
Erdtman, G. On pollegrains and dinoflagellate cysts in the firth of Gullmaren, S. W. Sweden. Botaniska Notiser 1954, 1954, 103–111.
[7]
Braarud, T. Morphological Observations on Marine Dinoflagellate Cultures (Porella Perforata, Goniaulax Tamarensis, Protoceratium Reticulatum); Dybwad: Oslo, Norway, 1945; pp. 1–18.
[8]
Nordli, E. Resting spores in Gonyaulax polyedra Stein. Nytt Mag. Naturvidenskapene 1951, 88, 207–212.
[9]
Von Stosch, H. Dinophyta; Springer Verlag: Berlin, Germany, 1967; Volume 18, pp. 626–636.
[10]
Von Stosch, H.A. La signification cytologique de la “cyclose nucleaire” dans le cycle de vie des dinoflagelles. Mem. Soc. Bot. Fr. 1972, 1972, 201–212.
[11]
Von Stosch, H.A. Sexualit?t bei Ceratium cornutum (dinophyta). Naturwissenschaften 1965, 52, 112–113, doi:10.1007/BF00626331.
[12]
Von Stosch, H.A. Observations on vegetative reproduction and sexual life cycles of two freshwater dinoflagellates, Gymondinium pseudopalustre Schiller and Woloszynskia apiculata sp. nov. Br. Phycol. 1973, 8, 105–134, doi:10.1080/00071617300650141.
[13]
Loeblich, A.I.; Loeblich, L. Dinoflagellate Cysts; Academic Press: New York, NY, USA, 1984.
[14]
Lenormand, T.; Otto, S. The evolution of recombination in a heterogeneous environment. Genetics 2000, 156, 423–438.
[15]
Lee, S.; Ni, M.; Li, W.; Shertz, C.; Heitman, J. The evolution of sex: A perspective from the fungal kingdom. Microbiol. Mol. Biol. Rev. 2010, 74, 298–340, doi:10.1128/MMBR.00005-10.
[16]
Wall, D. Modern hystrichospheres and dinoflagellate cysts from the Woods Hole region. Grana Palynol. 1965, 6, 297–314, doi:10.1080/00173136509429150.
[17]
Steidinger, K. Implications of dinoflagellate life cycles on initiation of Gymnodinium breve red tides. Environ. Lett. 1975, 9, 129–139, doi:10.1080/00139307509435842.
[18]
Anderson, D.M.; Wall, D. Potential importance of benthic cysts of Gonyaulax tamarensis and G. excavata in initiating toxic dinoflagellate blooms. J. Phycol. 1978, 14, 224–234, doi:10.1111/j.1529-8817.1978.tb02452.x.
[19]
Uchida, T. Sexual reproduction of Scrippsiella trochoidea isolated from Muroran Harbor Hokkaido. Bull. Jpn. Soc. Sci. Fish. 1991, 57, 1215, doi:10.2331/suisan.57.2249.
[20]
Uchida, T.; Matsuyama, Y.; Yamaguchi, M.; Honjo, T. The life cycle of Gyrodinium instriatum (Dinophyceae) in culture. Phycol. Res. 1996, 44, 119–123, doi:10.1111/j.1440-1835.1996.tb00040.x.
[21]
Figueroa, R.I.; Bravo, I. A study of the sexual reproduction and determination of mating type of Gymnodinium nolleri (Dinophyceae) in culture. J. Phycol. 2005, 41, 74–83, doi:10.1111/j.1529-8817.2005.04045.x.
[22]
Figueroa, R.I.; Bravo, I. Sexual reproduction and two different encystment strategies of Lingulodinium polyedrum (Dinophyceae) in culture. J. Phycol. 2005, 41, 370–379, doi:10.1111/j.1529-8817.2005.04150.x.
[23]
Figueroa, R.I.; Bravo, I.; Garcés, E. Multiples routes of sexuality in Alexandrium taylori (Dinophyceae) in culture. J. Phycol. 2006, 42, 1028–1039, doi:10.1111/j.1529-8817.2006.00262.x.
[24]
Figueroa, R.I.; Bravo, I.; Garcés, E.; Ramilo, I. Nuclear features and effect of nutrients on Gymnodinium catenatum (Dinophyceae) sexual stages. J. Phycol. 2006, 42, 67–77, doi:10.1111/j.1529-8817.2006.00181.x.
[25]
Kremp, A.; Parrow, M. Evidence for asexual resting cysts in the life cycle of the marine peridinoid dinoflagellate, Scrippsiella hangoei. J. Phycol. 2006, 42, 400–409, doi:10.1111/j.1529-8817.2006.00205.x.
[26]
Parrow, M.W.; Burkholder, J.M. The sexual life cycles of Pfiesteria piscicida and cryptoperidiniopsoids (Dinophyceae). J. Phycol. 2004, 40, 664–673, doi:10.1111/j.1529-8817.2004.03202.x.
[27]
Dale, B. Cysts of the toxic red-tide dinoflagellate Gonyaulax excavata (Braarud) Balech from Oslofjorden, Norway. Sarsia 1977, 63, 29–34.
[28]
Taylor, F.J.R. On dinoflagellate evolution. BioSystems 1980, 13, 65–108, doi:10.1016/0303-2647(80)90006-4.
[29]
Fritsch, F.E. The Structure and Reproduction of the Algae; Cambridge University Press: London, UK, 1935; Volume I.
[30]
Dale, B. Dinoflagellate Resting Cysts. In Survival Strategies of the Algae; Frixell, G.A., Ed.; Cambridge University Press: New York, NY, USA, 1983; pp. 67–136.
[31]
Bravo, I.; Figueroa, R.; Garcés, E.; Fraga, S.; Massanet, A. The intricacies of dinoflagellate pellicle cysts: The example of Alexandrium minutum cysts from a bloom-recurrent area (Bay of Baiona, NW Spain). Deep Sea Res. Pt. II Top. Stud. Oceanogr. 2010, 57, 166–174, doi:10.1016/j.dsr2.2009.09.003.
[32]
Kita, T.; Fukuyo, Y.; Tokuda, H.; Hirano, R. Life history and ecology of Goniodoma pseudogoniaulax (Pyrrhophyta) in a rockpool. Bull. Mar. Sci. 1985, 37, 643–651.
[33]
Garcés, E.; Masó, M.; Camp, J. Role of temporary cysts in the population dynamics of Alexandrium taylori (Dinophyceae). J. Plankton Res. 2002, 24, 681–686, doi:10.1093/plankt/24.7.681.
[34]
Lindberg, K.; Moestrup, ?.; Daugbjerg, N. Studies on woloszynskioid dinoflagellates I: Woloszynskia coronata re-examined using light and electron microscopy and partial LSU rDNA sequences, with description of Tovellia gen. nov. and Jadwigia gen. nov. (Tovelliaceae fam. nov.). Phycologia 2005, 44, 416–440, doi:10.2216/0031-8884(2005)44[416:SOWDIW]2.0.CO;2.
[35]
Gribble, K.E.; Anderson, D.M.; Coats, D.W. Sexual and asexual processes in Protoperidinium steidingerae Balech (Dinophyceae), with observations on life-history stages of Protoperidinium depressum (Bailey) Balech (Dinophyceae). J. Eukaryot. Microbiol. 2009, 56, 88–103, doi:10.1111/j.1550-7408.2008.00378.x.
[36]
Figueroa, R.I.; Bravo, I.; Fraga, S.; Garces, E.; Llaveria, G. The life history and cell cycle of Kryptoperidinium foliaceum, a dinoflagellate with two eukaryotic nuclei. Protist 2009, 160, 285–300, doi:10.1016/j.protis.2008.12.003.
[37]
Litaker, R.W.; Vandersea, M.W.; Kibler, S.R.; Madden, V.J.; Noga, E.J.; Tester, P.A. Life cycle of the heterotrophic dinoflagellate Pfiesteria piscicida (Dinophyceae). J. Phycol. 2002, 38, 442–463.
[38]
Zeng, N.; Gu, H.; Smith, K.F.; Rhodes, L.L.; Selwood, A.I.; Yang, W. The first report of Vulcanodinium rugosum (Dinophyceae) from the South China Sea with a focus on the life cycle. N. Z. J. Mar. Freshw. Res. 2012, 46, 511–521, doi:10.1080/00288330.2012.719911.
[39]
Evitt, W.R. Observations on the morphology of fossil dinoflagellates. Micropaleontology 1961, 7, 385–420, doi:10.2307/1484378.
[40]
Evitt, W.R. Dinoflagellates and Other Organisms in Palynological Preparations. In Aspects of Palynology; Tschudy, R.H., Scott, R.A., Eds.; Wiley-Interscience: New York, NY, USA, 1969; pp. 439–479.
[41]
Harland, R. A summary review of the morphology and classification of the fossil peridiniales (dinoflagellates) with respect to their modern representatives. Geophytology 1971, 1, 135–150.
Williams, G.L.; Sarjeant, W.A.S.; Kidson, E.J. A Glossary of the Terminology Applied to Dinoflagellate Amphiesmae and Cysts and Acritarchs; American Association of Stratigraphic Palynologists: Houston, TX, USA, 1978; Volume 2, pp. 1–121.
[44]
Matsuoka, K.; Fukuyo, Y.; Anderson, D. Methods for Modern Dinoflagellate Cyst Studies. In Red Tides: Biology, Environmental Science and Toxicology; Okaichi, T., Anderson, D.M., Nemoto, K., Eds.; Elsevier: New York, NY, USA, 1989; pp. 461–479.
[45]
Matsuoka, K.; Fukuyo, Y. Technical Guide for Modern Dinoflagellate Cyst Study; WESTPAC-HAB/WESTPAC/IOC: Tokio, Japan, 2000; p. 75.
[46]
Mertens, K.N.; Ribeiro, S.; Bouimetarhan, I.; Caner, H.; Nebout, N.C.; Dale, B.; De Vernal, A.; Ellegaard, M.; Filipova, M.; Godhe, A.; et al. Process length variation in cysts of a dinoflagellate, Lingulodinium machaerophorum, in surface sediments: Investigating its potential as salinity proxy. Mar. Micropaleontol. 2009, 70, 54–69, doi:10.1016/j.marmicro.2008.10.004.
[47]
Kokinos, J.P.; Anderson, D.M. Morphological development of resting cysts in cultures of the marine dinoflagellate Lingulodinium polyedrum (=L. machaerophorum). Palynology 1995, 19, 143–166.
[48]
Bibby, B.T.; Dodge, J.D. The encystment of a freshwater dinoflagellate: A light and electron-microscopical study. Br. Phycol. J. 1972, 7, 85–100.
[49]
Dürr, V.G. Electron microscope studies on the theca of dinoflagellates. 3. The cysts of Peridinium cinctum. Arch. Protistenkd. 1979, 122, 121–139, doi:10.1016/S0003-9365(79)80022-6.
[50]
De Leeuw, J.; Versteegh, G.; van Bergen, P. Biomacromolecules of algae and plants and their fossil analogues. Plant Ecol. 2006, 182, 209–233.
[51]
Kokinos, J.P.; Eglinton, T.I.; Go?i, M.A.; Boon, J.J.; Martoglio, P.A.; Anderson, D.M. Characterization of a highly resistant biomacromolecular material in the cell wall of a marine dinoflagellate resting cyst. Org. Geochem. 1998, 28, 265–288, doi:10.1016/S0146-6380(97)00134-4.
[52]
Versteegh, G.; Blokker, P.; Wood, G.; Collinson, M.; Damste, J.; de Leeuw, J. An example of oxidative polymerization of unsaturated fatty acids as a preservation pathway for dinoflagellate organic matter. Org. Geochem. 2004, 35, 1129–1139, doi:10.1016/j.orggeochem.2004.06.012.
[53]
Versteegh, G.; Blokker, P.; Bogus, K.; Harding, I.; Lewis, J.; Oltmanns, S.; Rochon, A.; Zonneveld, K. Infra red spectroscopy, flash pyrolysis, thermally assisted hydrolysis and methylation (THM) in the presence of tetramethylammonium hydroxide (TMAH) of cultured and sediment-derived Lingulodinium polyedrum (Dinoflagellata) cyst walls. Org. Geochem. 2012, 43, 92–102, doi:10.1016/j.orggeochem.2011.10.007.
[54]
Taylor, F.J.R. Dinoflagellate Morphology. In The Biology of Dinoflagellates; Taylor, F.J.R., Ed.; Blackwell Scientific Publications: Oxford, UK, 1987; Volume 21, pp. 24–91.
[55]
Loeblich, A.R.I. The Amphiesma or Dinoflagellate Cell Covering. In Proceedings of the North American Paleontological Convention: Field Museum of Natural History, Chicago, IL, USA, 5–7 September, 1970; Yochelson, E.L., Ed.; Allen Press: Lawrence, KS, USA, 1971; Volume 2, pp. 867–929.
[56]
Morrill, L.C.; Loeblich, A.R. The dinoflagellate pellicular wall layer and its occurrence in the Division Pyrrhophyta. J. Phycol. 1981, 17, 315–323, doi:10.1111/j.1529-8817.1981.tb00857.x.
[57]
H?hfeld, I.; Melkonian, M. Amphiesmal ultrastructure of dinoflagellates: A reevaluation of pellicle formation. J. Phycol. 1992, 28, 82–89.
[58]
Gao, X.P.; Dodge, J.D.; Lewis, J. An ultrastructural-study of planozygotes and encystment of a marine dinoflagellate, Scrippsiella sp. Br. Phycol. J. 1989, 24, 153–165.
[59]
Chapman, D.V.; Dodge, J.D.; Heaney, S.I. Cyst formation in the fresh-water dinoflagellate Ceratium hirundinella (Dinophyceae). J. Phycol. 1982, 18, 121–129, doi:10.1111/j.1529-8817.1982.tb03165.x.
[60]
Fritz, L.; Anderson, D.M.; Triemer, R.E. Ultrastructural aspects of sexual reproduction in the red tide dinoflagellate Gonyaulax tamarensis. J. Phycol. 1989, 25, 95–107, doi:10.1111/j.0022-3646.1989.00095.x.
[61]
Kennaway, G.M.; Lewis, J.M. An ultrastructural study of hypnozygotes of Alexandrium species (Dinophyceae). Phycologia 2004, 43, 353–363.
[62]
Bravo, I.; Garces, E.; Diogene, J.; Fraga, S.; Sampedro, N.; Figueroa, R.I. Resting cysts of the toxigenic dinoflagellate genus Alexandrium in recent sediments from the Western Mediterranean Coast, including the first description of cysts of A. kutnerae and A. peruvianum. Eur. J. Phycol. 2006, 41, 293–302, doi:10.1080/09670260600810360.
[63]
Mertens, K.N.; Bringue, M.; van Nieuwenhove, N.; Takano, Y.; Pospelova, V.; Rochon, A.; de Vernal, A.; Radi, T.; Dale, B.; Patterson, R.T.; et al. Process length variation of the cyst of the dinoflagellate Protoceratium reticulatum in the North Pacific and Baltic-Skagerrak region: Calibration as an annual density proxy and first evidence of pseudo-cryptic speciation. J. Quat. Sci. 2012, 27, 734–744, doi:10.1002/jqs.2564.
[64]
Ellegaard, M.; Lewis, J.; Harding, I. Cyst-theca relationship, life cycle, and effects of temperature and salinity on the cyst morphology of Gonyaulax baltica sp nov (Dinophyceae) from the Baltic Sea area. J. Phycol. 2002, 38, 775–789, doi:10.1046/j.1529-8817.2002.01062.x.
[65]
Zonneveld, K.A.F.; Susek, E. Effects of temperature, light and salinity on cyst production and morphology of Tuberculodinium vancampoae (the resting cyst of Pyrophacus steinii). Rev. Palaeobot. Palynol. 2007, 145, 77–88, doi:10.1016/j.revpalbo.2006.09.001.
[66]
Hallett, R.I. Consequences of Environmental Change on the Growth and Morphology of Lingulodinium polyedrum (Dinophyceae) in Culture. Ph.D. Thesis, University of Westminster, London, UK, 1999.
[67]
Wall, D. Biological problems concerning fossilizable dinoflagellates. Geosci. Man 1971, 3, 1–15, doi:10.1080/00721395.1971.9989704.
[68]
Anderson, D.M. The Roles of Dormant Cysts in Toxic Dinoflagellate Blooms and Shellfish Toxicity. In Seafood Toxins; Ragelis, E.P., Ed.; American Chemical Society: Washington, DC, USA, 1984; Volume 262, pp. 125–138.
[69]
Pouchet, G. Contribution à l’histoire des ciclioflagellés. J. Anat. Physiol. 1883, 19, 399–455.
[70]
Biecheler, B. Recherches sur les péridiniens. Bull. Biol. Fr. Belg. 1952, 36 (Suppl.), 1–149.
Figueroa, R.I.; Garces, E.; Bravo, I. Comparative study of the life cycles of Alexandrium tamutum and Alexandrium minutum (Gonyaulacales, Dinophyceae) in culture. J. Phycol. 2007, 43, 1039–1053, doi:10.1111/j.1529-8817.2007.00393.x.
[73]
Figueroa, R.I.; Rengefors, K.; Bravo, I. Effects of parental factors and meiosis on sexual offspring of Gymnodinium nolleri (Dinophyceae). J. Phycol. 2006, 42, 350–362, doi:10.1111/j.1529-8817.2006.00191.x.
[74]
Kühn, S.F.; Medlin, L.K. The systematic position of the parasitoid marine dinoflagellate Paulsenella vonstoschii (Dinophyceae) inferred from nuclear-encoded small subunit ribosomal DNA. Protist 2005, 156, 393–398, doi:10.1016/j.protis.2005.09.002.
[75]
Alpermann, T.J.; Beszteri, B.; John, U.; Tillmann, U.; Cembella, A.D. Implications of life-history transitions on the population genetic structure of the toxigenic marine dinoflagellate Alexandrium tamarense. Mol. Ecol. 2009, 18, 2122–2133.
[76]
Miyazono, A.; Nagai, S.; Kudo, I.; Tanizawa, K. Viability of Alexandrium tamarense cysts in the sediment of Funka Bay, Hokkaido, Japan: Over a hundred year survival times for cysts. Harmful Algae 2012, 16, 81–88, doi:10.1016/j.hal.2012.02.001.
[77]
Pfiester, L.A.; Anderson, D.M. Dinoflagellate Reproduction. In The Biology of Dinoflagellates; Taylor, F.J.R, Ed.; Blackwell Scientific: Oxford, UK, 1987; pp. 611–648.
[78]
Anderson, D.M.; Lindquist, N.L. Time-course measurements of phosphorus depletion and cyst formation in the dinoflagellate Gonyaulax tamarensis Lebour. J. Exp. Mar. Biol. Ecol. 1985, 86, 1–13, doi:10.1016/0022-0981(85)90039-5.
[79]
Anderson, D.M.; Coats, D.W.; Tyler, M.A. Encystment of the dinoflagellate Gyrodinium uncatenum temperatura and nutrient effect. J. Phycol. 1985, 21, 200–206, doi:10.1111/j.0022-3646.1985.00200.x.
[80]
Rengefors, K.; Anderson, D.M. Environmental and endogenous regulation of cyst germination in two freshwater dinoflagellates. J. Phycol. 1998, 34, 568–577.
[81]
Grzebyk, D.; Berland, B. Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from the Mediterranean Sea. J. Plankton Res. 1996, 18, 1837–1849, doi:10.1093/plankt/18.10.1837.
[82]
Figueroa, R.I.; Bravo, I.; Garces, E. Effects of nutritional factors and different parental crosses on the encystment and excystment of Alexandrium catenella (Dinophyceae) in culture. Phycologia 2005, 44, 658–670.
[83]
Anderson, D.M.; Taylor, C.D.; Armbrust, E.V. The effect of darkness and anaerobiosis on dinoflagellate cyst germination. Limnol. Oceanogr. 1987, 32, 340–351, doi:10.4319/lo.1987.32.2.0340.
[84]
Bravo, I.; Anderson, D.M. The effects of temperatura, growth-medium and darkness on excystment and growth of the toxic dinoflagellate Gymnodinium catenatum from northwest Spain. J. Plankton Res. 1994, 16, 513–525, doi:10.1093/plankt/16.5.513.
[85]
Kremp, A.; Anderson, D.M. Factors regulating germination of resting cysts of the spring bloom dinoflagellate Scrippsiella hangoei from the Northern Baltic Sea. J. Plankton Res. 2000, 22, 1311–1327, doi:10.1093/plankt/22.7.1311.
[86]
Lundgren, V.; Graneli, E. Influence of altered light conditions and grazers on Scrippsiella trochoidea (Dinophyceae) cyst formation. Aquat. Microb. Ecol. 2011, 63, 231–243, doi:10.3354/ame01497.
[87]
Rintala, J.M.; Spilling, K.; Blomster, J. Temporary cyst enables long-term dark survival of Scrippsiella hangoei (Dinophyceae). Mar. Biol. 2007, 152, 57–62, doi:10.1007/s00227-007-0652-x.
[88]
Fistarol, G.O.; Legrand, C.; Rengefors, K.; Graneli, E. Temporary cyst formation in phytoplankton: A response to allelopathic competitors? Environ. Microbiol. 2004, 6, 791–798, doi:10.1111/j.1462-2920.2004.00609.x.
[89]
Tillmann, U.; John, U.; Cembella, A. On the allelochemical potency of the marine dinoflagellate Alexandrium ostenfeldii against heterotrophic and autotrophic protists. J. Plankton Res. 2007, 29, 527–543, doi:10.1093/plankt/fbm034.
[90]
Montresor, M.; Nuzzo, L.; Mazzocchi, M.G. Viability of dinoflagellate cysts after the passage through the copepod gut. J. Exp. Mar. Biol. Ecol. 2003, 287, 209–221, doi:10.1016/S0022-0981(02)00549-X.
[91]
Laabir, M.; Amzil, Z.; Lassus, P.; Masseret, E.; Tapilatu, Y.; de Vargas, R.; Grzebyk, D. Viability, growth and toxicity of Alexandrium catenella and Alexandrium minutum (Dinophyceae) following ingestion and gut passage in the oyster Crassostrea gigas. Aquat. Living Resour. 2007, 20, 51–57, doi:10.1051/alr:2007015.
[92]
Toth, G.B.; Noren, F.; Selander, E.; Pavia, H. Marine dinoflagellates show induced life-history shifts to escape parasite infection in response to water-borne signals. Proc. R. Soc. B Biol. Sci. 2004, 271, 733–738, doi:10.1098/rspb.2003.2654.
[93]
Figueroa, R.I.; Garces, E.; Massana, R.; Camp, J. Description, host-specificity, and strain selectivity of the dinoflagellate parasite Parvilucifera sinerae sp nov (Perkinsozoa). Protist 2008, 159, 563–578, doi:10.1016/j.protis.2008.05.003.
[94]
Chambouvet, A.; Alves-de-Souza, C.; Cueff, V.; Marie, D.; Karpov, S.; Guillou, L. Interplay between the parasite Amoebophrya sp. (Alveolata) and the cyst formation of the red tide dinoflagellate Scrippsiella trochoidea. Protist 2011, 162, 637–649, doi:10.1016/j.protis.2010.12.001.
[95]
Wall, D. Taxonomy and Cysts of Red-Tide Dinoflagellates. In Proceedings of the First International Conference on Toxic Dinoflagellate Blooms, Boston, MA, USA, November 1974; Lo Cicero, V.R., Ed.; Massachusetts Science and Technology Foundation: Wakefield, MA, USA, 1975; pp. 249–255.
[96]
Anderson, D.M. Effects of temperature conditioning on development and germination of Gonyaulax tamarensis (Dinophyceae) hypnozygotes. J. Phycol. 1980, 16, 166–172.
[97]
Reynolds, C.S. The Ecology of Freshwater Phytoplankton; Cambridge University Press: London, UK, 1984.
[98]
Anderson, D.M.; Keafer, B.A. An endogenous annual clock in the toxic marine dinoflagellate Gonyaulax tamarensis. Nature 1987, 325, 616–617, doi:10.1038/325616a0.
[99]
Anderson, D.M. Physiology and Bloom Dynamics of Toxic Alexandrium Species, with Emphasis on Life Cycle Transitions. In Physiological Ecology of Harmful Algal Blooms; Anderson, D.M., Cembella, A.D., Hallegraeff, G.M., Eds.; Springer-Verlag: Heidelberg, Germany, 1998; Volume 41, pp. 29–47.
[100]
Steidinger, K.; Haddad, K. Biologic and hydrographic aspects of red tides. BioScience 1981, 31, 814–819, doi:10.2307/1308678.
[101]
Heiskanen, A.S. Mass encystment and sinking of dinoflagellates during a spring bloom. Mar. Biol. 1993, 116, 161–167, doi:10.1007/BF00350743.
[102]
Kremp, A. Effects of cyst resuspension on germination and seeding of two bloom-forming dinoflagellates in the Baltic Sea. Mar. Ecol. Prog. Ser. 2001, 216, 57–66, doi:10.3354/meps216057.
[103]
Spilling, K.; Kremp, A.; Tamelander, T. Vertical distribution and cyst production of Peridiniella catenata (Dinophyceae) during a spring bloom in the Baltic Sea. J. Plankton Res. 2006, 28, 659–665, doi:10.1093/plankt/fbi149.
[104]
Lundholm, N.; Ribeiro, S.; Andersen, T.; Koch, T.; Godhe, A.; Ekelund, F.; Ellegaard, M. Buried alive-germination of up to a century-old marine protist resting stages. Phycologia 2011, 50, 629–640, doi:10.2216/11-16.1.
[105]
Ribeiro, S.; Berge, T.; Lundholm, N.; Andersen, T.; Abrantes, F.; Ellegaard, M. Phytoplankton growth after a century of dormancy illuminates past resilience to catastrophic darkness. Nat. Commun. 2011, 2, doi:10.1038/ncomms1314.
[106]
Smayda, T.; Trainer, V. Dinoflagellate blooms in upwelling systems: Seeding, variability, and contrasts with diatom bloom behaviour. Prog. Oceanogr. 2010, 85, 92–107, doi:10.1016/j.pocean.2010.02.006.
[107]
Garcés, E.; Masó, M.; Camp, J. A recurrent and localized dinoflagellate bloom in Mediterranean beach. J. Plankton Res. 1999, 21, 2373–2391, doi:10.1093/plankt/21.12.2373.
[108]
Basterretxea, G.; Garcés, E.; Masó, M.; Jordi, A.; Masó, M.; Tintoré, J. Breeze conditions as a favoring mechanism of Alexandrium taylori blooms at a Mediterranean beach. Estuar. Coast. Mar. Sci. 2005, 62, 1–12.
[109]
Bravo, I.; Fraga, S.; Figueroa, R.I.; Pazos, Y.; Massanet, A.; Ramilo, I. Bloom dynamics and life cycle strategies of two toxic dinoflagellates in a coastal upwelling system (NW Iberian Peninsula). Deep Sea Res. Pt. II Top. Stud. Oceanogr. 2010, 57, 222–234.
[110]
Figueroa, R.I.; Bravo, I.; Ramilo, I.; Pazos, Y.; Angeles, M. New life-cycle stages of Gymnodinium catenatum (Dinophyceae): Laboratory and field observations. Aquat. Microb. Ecol. 2008, 52, 13–23, doi:10.3354/ame01206.
[111]
Kim, C.H.; Cho, H.J.; Shin, J.B.; Moon, C.H.; Matsuoka, K. Regeneration from hyaline cysts of Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae). A red tide organism along the Korean Coast. Phycologia 2002, 41, 667–669, doi:10.2216/i0031-8884-41-6-667.1.
[112]
Bravo, I.; Vila, M.; Casabianca, S.; Rodriguez, F.; Rial, P.; Riobó, P.; Penna, A. Life cycle stages of the benthic palytoxin-producing dinoflagellate Ostreopsis cf. ovata (Dinophyceae). Harmful Algae 2012, 18, 24–34, doi:10.1016/j.hal.2012.04.001.
[113]
Salgado, P.; Pizarro, G.; Guzmán, L.; Bravo, I. Primer Registro de Células de Resistencia del Dinoflagelado Prorocentrum lima en Sedimentos de la Costa Austral de Chile. In Proceedings of the XXX Congreso de Ciencias del Mar, Concepción, Chile, 19–22 October 2010.
McNown, J.S.; Malaika, J. Effects of particle shape on settling velocity at low reynolds numbers. Trans. Am. Geophys. Union 1950, 31, 74–82, doi:10.1029/TR031i001p00074.
[118]
Belmonte, G.; Miglietta, A.; Rubino, F.; Boero, F. Morphological convergence of resting stages of planktonic organisms: A review. Hydrobiologia 1997, 355, 159–165, doi:10.1023/A:1003071205424.