Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-25T02:35:23.131Z Has data issue: false hasContentIssue false
  • English
  • Français

The cyst of the calcareous dinoflagellate Scrippsiella trifida: Resolving the fossil record of its organic wall by that of Alexandrium tamarense

Published online by Cambridge University Press:  20 May 2016

Martin J. Head ,
Jane Lewis  and
Anne de Vernal
Martin J. Head
Affiliation:
Godwin Institute for Quaternary Research, Department of Geography, University of Cambridge, Downing Place, Cambridge CB2 3EN, United Kingdom
Jane Lewis
Affiliation:
School of Biosciences, University of Westminster, 115 New Cavendish Street, London W1W 6UW, United Kingdom,
Anne de Vernal
Affiliation:
GEOTOP, Université du Québec à Montréal, C.P. 8888, Montréal H3C 3P8, Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

Scrippsiella trifida Lewis, 1991 ex Head, 1996 is a nontoxic marine calciodinelloidean dinoflagellate whose resting cyst has a distinctive wall containing large, erect, trifurcate, recurving calcareous processes that separate two organic layers. We show that the organic wall layers of living Scrippsiella trifida cysts are resistant to acetolysis and can therefore potentially fossilize, and we report on abundant Scrippsiella trifida cysts from latest Pleistocene and early Holocene marine sediments off eastern Canada, representing the first confirmed fossil discovery of this species in the North Atlantic. A reappraisal of late Quaternary palynological records now shows that the organic remains of Scrippsiella trifida cysts have been widely misidentified as cysts of Alexandrium tamarense (Lebour, 1925) Balech, 1985, a goniodomacean (and hence noncalcareous) dinoflagellate and major cause of paralytic shellfish poisoning in humans. The morphology of these two cyst types is contrasted, and the modern and fossil distribution of Scrippsiella trifida cysts in sediments of the North Atlantic and adjacent areas is now clarified. It is apparent from this distribution that Scrippsiella trifida favors neritic environments characterized by cool winters and relatively warm (14°–25°C) summers. Extremely high fluxes of S. trifida cysts in nearshore areas off Nova Scotia and southern Greenland during deglaciation and early postglacial time (14–7 ka) have no modern analog but may signal a reduction in salinity caused by meltwater discharge. In general, the organic walls of calcareous dinoflagellate cysts are more common components of palynological assemblages than hitherto realized.

Type
Research Article
Information
Journal of Paleontology , Volume 80 , Issue 1 , January 2006 , pp. 1 - 18
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, D. M. 1998. Physiology and bloom dynamics of toxic Alexandrium species, with emphasis on life cycle transitions, p. 29–48. In Anderson, D. M., Cembella, A. D., and Hallegraeff, G. M. (eds.), Physiological Ecology of Harmful Algal Blooms. NATO-Advanced Study Institute Series, G 41. Springer-Verlag, Berlin.Google Scholar
Anderson, D. M., and Wall, D. 1978. Potential importance of benthic cysts of Gonyaulax tamarensis and G. excavata in initiating toxic dinoflagellate blooms. Journal of Phycology, 14:224–234.Google Scholar
Anderson, D. M., Kulis, D. M., Doucette, G. J., Gallagher, J. C., and Balech, E. 1994. Biogeography of toxic dinoflagellates in the genus Alexandrium from the northeastern United States and Canada. Marine Biology, 120:467–478.Google Scholar
Balech, E. 1959. Two new genera of dinoflagellates from California. The Biological Bulletin, 116:195–203.Google Scholar
Balech, E. 1967. Dinoflagelados nuevos o interesantes del Golfo de México y Caribe. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” e Instituto Nacional de Investigación de las Ciencias Naturales, Hidrobiología, 2(3):77–126.Google Scholar
Balech, E. 1971. Microplancton del Atlantico Ecuatorial Oeste (Equalant I). Servicio de Hidrografia Naval, Buenos Aires H, 654:1–103.Google Scholar
Balech, E. 1985. The genus Alexandrium or Gonyaulax of the tamarensis group, p. 33–38. In Anderson, D. M., White, A. W., and Baden, D. G. (eds.), Toxic Dinoflagellates. Elsevier, New York.Google Scholar
Balech, E. 1990. Four new dinoflagellates. Helgoländer Meeresuntersuchungen, 44:387–396.Google Scholar
Balech, E. 1994. Three new species of the genus Alexandrium (Dinoflagellata). Transactions of the American Microscopical Society, 113:216–220.CrossRefGoogle Scholar
Balech, E. 1995. The Genus Alexandrium Halim (Dinoflagellata). Sherkin Island Marine Station, Cork, Ireland, Special Publication, iii + 151 p.Google Scholar
Balech, E., and Tangen, K. 1985. Morphology and taxonomy of toxic species in the tamarensis group (Dinophyceae) Alexandrium excavatum (Braarud) comb. nov. and Alexandrium ostenfeldii (Paulsen) comb. nov. Sarsia, 70:333–343.Google Scholar
Berger, A., and Loutre, M. F. 2002. An exceptionally long interglacial ahead? Science, 297:1287–1288.Google Scholar
Bertini, A., de Vernal, A., Hillaire-Marcel, C., and Bilodeau, G. 1998. Palaeoceanographical changes in the northwest North Atlantic since ca. 20 ka based on dinocyst assemblages. In Smelror, M. (ed.), Abstracts from the Sixth International Conference on Modern and Fossil Dinoflagellates Dino 6, Trondheim, June 1998. Norges teknisk-na-turvitenskapelige universitet Vitenskapsmuseet, Rapport botanisk serie, 1998–1–14–15.Google Scholar
Binder, B. J., and Anderson, D. M. 1987. Physiological and environmental control of germination in Scrippsiella trochoidea (Dinophyceae) resting cysts. Journal of Phycology, 23:99–107.Google Scholar
Binder, B. J., and Anderson, D. M. 1990. Biochemical composition and metabolic activity of Scrippsiella trochoidea (Dinophyceae) resting cysts. Journal of Phycology, 26:289–298.Google Scholar
Braarud, T. 1945. Morphological observations on marine dinoflagellate cultures (Porella perforata, Goniaulax tamarensis, Protoceratium reticulatum). Avhandlinger utgitt av Det Norske Videnskaps-Akademi i Oslo. I. Matematisk-Naturvidenskapelig Klasse, 1944(11), 18 p.Google Scholar
Bütschli, O. 1885. Protozoa, p. 865–1088. In Dr. H. G. Bronn's Klassen und Ordnungen des Thier-Reiches, wissenschaftlich dargestellt in Wort und Bild. Erster Band. C. F. Winter'sche Verlagshandlung, Leipzig.Google Scholar
Cembella, A. D., Lewis, N. I., and Quilliam, M. A. 2000. The marine dinoflagellate Alexandrium ostenfeldii (Dinophyceae) as the causative organism of spirolide shellfish toxins. Phycologia, 39:67–74.Google Scholar
Cembella, A. D., Quilliam, M. A., Lewis, N. I., Bauder, A. G., Dell'Aversano, C., Thomas, K., Jellett, J., and Cusack, R. R. 2002. The toxigenic marine dinoflagellate Alexandrium tamarense as the probable cause of mortality of caged salmon in Nova Scotia. Harmful Algae, 1:313–325.CrossRefGoogle Scholar
Cho, Hyun-Jin, and Matsuoka, K. 2001. Distribution of dinoflagellate cysts in surface sediments from the Yellow Sea and East China Sea. Marine Micropaleontology, 42:103–123.Google Scholar
Dale, B. 1976. Cyst formation, sedimentation, and preservation: Factors affecting dinoflagellate assemblages in Recent sediments from Tron-dheimsfjord, Norway. Review of Palaeobotany and Palynology, 22:39–60.Google Scholar
Dale, B. 1977. Cysts of the toxic red-tide dinoflagellate Gonyaulax excavata (Braarud) Balech from Oslofjorden, Norway. Sarsia, 63:29–34. (Imprinted, 1978)Google Scholar
Dale, B. 1983. Dinoflagellate resting cysts: “Benthic plankton,” p. 69–136. In Fryxell, G. A. (ed.), Survival Strategies of the Algae. Cambridge University Press, Cambridge, United Kingdom.Google Scholar
Damassa, S. P. 1998. A hole-y alliance: Calciodinelloidean archeopyles in dinosporin cysts. Palynology, 22:238.Google Scholar
de Vernal, A., and Hillaire-Marcel, C. 2000. Sea-ice cover, sea-surface salinity and halo-/thermocline structure of the northwest North Atlantic: Modern versus full glacial conditions. Quaternary Science Reviews, 19:65–85.Google Scholar
de Vernal, A., Guiot, J., and Turon, J.-L. 1993. Late and postglacial paleoenvironments of the Gulf of St. Lawrence: Marine and terrestrial palynological evidence. Géographie physique et Quaternaire, 47:167–180.Google Scholar
de Vernal, A., Hillaire-Marcel, C., and Bilodeau, G. 1996. Reduced meltwater outflow from the Laurentide ice margin during the Younger Dryas. Nature, 381:774–777.Google Scholar
de Vernal, A., Turon, J.-L., and Guiot, J. 1994. Dinoflagellate cyst distribution in high-latitude marine environments and quantitative reconstruction of sea-surface salinity, temperature, and salinity. Canadian Journal of Earth Sciences, 31:48–62.Google Scholar
de Vernal, A., Hillaire-Marcel, C., Turon, J.-L., and Matthiessen, J. 2000. Reconstruction of sea-surface temperature, salinity, and seaice cover in the northern North Atlantic during the last glacial maximum based on dinocyst assemblages. Canadian Journal of Earth Sciences, 37:725–750.Google Scholar
de Vernal, A., Rochon, A., Turon, J.-L., and Matthiessen, J. 1997. Organic-walled dinoflagellate cysts: Palynological tracers of sea-surface conditions in middle to high latitude marine environments. Geobios, 30:905–920.Google Scholar
de Vernal, A., Eynaud, F., Henry, M., Hillaire-Marcel, C., Londeix, L., Mangin, S., Matthiessen, J., Marret, F., Radi, T., Rochon, A., Solignac, S., and J.-L. Turon. 2005. Reconstruction of sea-surface conditions at middle to high latitudes of the Northern Hemisphere during the Last Glacial Maximum (LGM) based on dinoflagellate cyst assemblages. Quaternary Science Reviews, 24:897–924.Google Scholar
de Vernal, A., Henry, M., Matthiessen, J., Mudie, P. J., Rochon, A., Boessenkool, K. P., Eynaud, F., Grøsfjeld, K., Guiot, J., Hamel, D., Harland, R., Head, M. J., Kunz-Pirrung, M., Levac, E., Loucheur, V., Peyron, O., Pospelova, V., Radi, T., Turon, J.-L., and Voronina, E. 2001. Dinoflagellate cyst assemblages as tracers of sea-surface conditions in the northern North Atlantic, Arctic and sub-Arctic seas: The new ‘n = 677’ database and its application for quantitative palaeoceanographic reconstruction. Journal of Quaternary Science, 16:681–698.CrossRefGoogle Scholar
Ehrenberg, C. G. 1831. Animalia evertebrata. In Hemprich, P. C. and Ehrenberg, C. G. (eds.), Symbolae physicae seu icones et descriptiones naturalium novorum aut minus cognitorum quae ex itineribus Lybiam Aegyptum Nubiam Dongalam Syriam Arabiam et Habessinian. Pars Zoologica. Abhandlungen der deutschen Akademie der Wissenschaften. (unpaginated)Google Scholar
Ellegaard, M., Christensen, N. F., and Moestrup, Ø. 1994. Dinoflagellate cysts from Recent Danish marine sediments. European Journal of Phycology, 29:183–194.CrossRefGoogle Scholar
Fensome, R. A., Taylor, F. J. R., Norris, G., Sarjeant, W. A. S., Wharton, D. I., and Williams, G. L. 1993. A Classification of Living and Fossil Dinoflagellates. Micropaleontology Special Publication, Number 7, 351 p.Google Scholar
Fritz, L., Anderson, D. M., and Triemer, R. E. 1989. Ultrastructural aspects of sexual reproduction in the red-tide dinoflagellate Gonyaulax tamarensis. Journal of Phycology, 25:95–107.CrossRefGoogle Scholar
Fukuyo, Y. 1980. Toxic plankton, p. 46–53. In Akashiwo Kenkyukai (= Research Group for Red Tide) (eds.), Recent Knowledge on the Red-Tide and Problems on Its Study. Nihon Suisan Shigen Hogo Kyokai, Tokyo.Google Scholar
Fukuyo, Y. 1985. Morphology of Protogonyaulax tamarensis (Lebour) Taylor and Protogonyaulax catenella (Whedon and Kofoid) Taylor from Japanese coastal waters. Bulletin of Marine Science, 37:529–537.Google Scholar
Fukuyo, Y., Sako, Y., Matsuoka, K., Imai, I., Takahashi, M., and Watanabe, M. 2003. Biological character of red-tide organisms, p. 61–178. In Okaichi, T. (ed.), Red Tides. Terra Scientific Publishing, Tokyo, and Kluwer Academic, Dordrecht.Google Scholar
Fütterer, D. 1978. Distribution of calcareous dinoflagellates in Cenozoic sediments of Site 366, eastern North Atlantic, p. 709–737. In Lancelot, Y., Seibold, E. et al. (eds.), Initial Reports of the Deep Sea Drilling Project, 41. (Imprinted 1977)Google Scholar
Gallagher, J. C. 1998. Genetic variation in harmful algal bloom species: An evolutionary ecology approach, p. 225–242. In Anderson, D. M., Cembella, A. D., and Hallegraeff, G. M. (eds.), Physiological Ecology of Harmful Algal Blooms. NATO-Advanced Study Institute Series, G 41. Springer-Verlag, Berlin.Google Scholar
Gao, Xiaoping, and Dodge, J. D. 1991. The taxonomy and ultrastructure of a marine dinoflagellate, Scrippsiella minima sp. nov. British Phycological Journal, 26:21–32.Google Scholar
Gao, Xiaoping, Dodge, J. D., and Lewis, J. 1989a. Gamete mating and fusion in the marine dinoflagellate Scrippsiella sp. Phycologia, 28:342–351.Google Scholar
Gao, Xiaoping, Dodge, J. D., and Lewis, J. 1989b. An ultrastructural study of planozygotes and encystment of a marine dinoflagellate, Scrippsiella sp. British Phycological Journal, 24:153–165.Google Scholar
Godhe, A., Norén, F., Kuylenstierna, M., Ekberg, C., and Karlson, B. 2001. Relationship between planktonic dinoflagellate abundance, cysts recovered in sediment traps and envrionmental factors in the Gull-mar Fjord, Sweden. Journal of Plankton Research, 23:923–938.Google Scholar
Haeckel, E. 1894. Systematische Phylogenie. Entwurf eines natürlichen Systems der Organismen auf Grand ihrer Stammesgeschichte, I. Systematische Phylogenie der Protisten und Pflanzen. Reimer, Berlin, xv + 400 p.Google Scholar
Halim, Y. 1960. Alexandrium minutum nov. g. nov. sp. Dinoflagellé provocant des “eaux rouges.” Vie et Milieu, 11:102–105.Google Scholar
Hallegraeff, G. M., and Bolch, C. J. 1992. Transport of diatom and dinoflagellate resting spores in ships' ballast water: Implications for plankton biogeography and aquaculture. Journal of Plankton Research, 14:1067–1084.Google Scholar
Hamer, J. P., Lucas, I. A. N., and McCollin, T. A. 2001. Harmful dinoflagellate resting cysts in ships' ballast tank sediments: Potential for introduction into English and Welsh waters. Phycologia, 40:246–255.Google Scholar
Head, M. J. 1996. Modern dinoflagellate cysts and their biological affinities, p. 1197–1248. In Jansonius, J. and McGregor, D. C. (eds.), Palynology: Principles and Applications. Vol. 3. American Association of Stratigraphic Palynologists Foundation, Dallas, Texas.Google Scholar
Head, M. J., and Westphal, H. 1999. Palynology and paleoenvironments of a Pliocene carbonate platform: The Clino Core, Bahamas. Journal of Paleontology, 73:1–25.Google Scholar
Hoppenrath, M., Elbrächter, M., Halliger, H., van Beusekom, J., and Drebes, G. 2004. Table 1: Phytoplankton: 1.2 Dinophyceae (dinoflagellates). In Flora and Fauna of the Northern Wadden Sea. Alfred Wegener Institute for Polar and Marine Research. http://www.awi-bremerhaven.de/Benthic/CoastalEco/list_of_species/index.html (accessed November 2004)Google Scholar
Horiguchi, T., and Chihara, M. 1983. Scrippsiella hexapraecingula sp. nov. (Dinophyceae), a tide pool dinoflagellate from the Northwest Pacific. Botanical Magazine, Tokyo, 96:351–358.Google Scholar
Hultberg, S. U. 1985a. Pithonella organica—a new calcareous dinoflagellate with an inner organic wall, p. 24–32. In Hultberg, S. U. (ed.), Dinoflagellate Studies of the Upper Maastrichtian and Danian in southern Scandinavia. Department of Geology, University of Stockholm,-Sweden (Published doctoral dissertation; republished as Hultberg, 1985b).Google Scholar
Hultberg, S. U. 1985b. Pithonella organica—a new calcareous dinoflagellate with an inner organic wall. Grana, 24:115–120.CrossRefGoogle Scholar
Indelicato, S. R., and Loeblich, A. R. III. 1986. A revision of the marine peridinioid genera (Pyrrhophyta) utilizing hypothecal-cingular plate relationships as a taxonomic guideline. The Japanese Journal of Phycology, 34:153–162.Google Scholar
Janofske, D. 1996. Ultrastructure types in Recent “calcispheres.” Bulletin de l'Institut océanographique, Monaco, 14:295–303, 427.Google Scholar
Janofske, D. 2000. Scrippsiella trochoidea and Scrippsiella regalis, nov. comb. (Peridiniales, Dinophyceae): A comparison. Journal of Phycology, 36:178–189.Google Scholar
Janofske, D., and Karwath, B. 2000. Oceanic calcareous dinoflagellates of the equatorial Atlantic Ocean: Cyst–theca relationship, taxonomy and aspects on ecology, p. 93–136. In Janofske, D. (ed.), Ecological studies on living and fossil calcareous dinoflagellates of the equatorial and tropical Atlantic Ocean. Berichte aus dem Fachbereich Geowissenschaften der Universität Bremen, Nr. 152.Google Scholar
John, U., Fensome, R. A., and Medlin, L. K. 2003. The application of a molecular clock based on molecular sequences and the fossil record to explain biogeographic distributions within the Alexandrium tamarense “species complex” (Dinophyceae). Molecular Biology and Evolution, 20:1015–1027.Google Scholar
Joyce, L. B. 2004. Dinoflagellate cysts in recent marine sediments from Scapa Flow, Orkney, Scotland. Botanica Marina, 47:173–183.Google Scholar
Kamptner, E. 1963. Coccolithineen-Skelettreste aus Tiefseeablagerungen des Pazifischen Ozeans. Annalen des Naturhistorischen Museums, Wien, 66:139–204.Google Scholar
Kennaway, G. M., and Lewis, J. M. 2004. An ultrastructural study of hypnozygotes of Alexandrium species (Dinophyceae). Phycologia, 43:353–363.Google Scholar
Kokinos, J. P., Eglinton, T. I., Goni, M. A., Boon, J. J., Martgolio, P. A., and Anderson, D. M. 1998. Characterization of a highly resistant biomacromolecular material in the cell wall of a marine dinoflagellate resting cyst. Organic Geochemistry, 28:265–288.Google Scholar
Lebour, M. V. 1925. The Dinoflagellates of Northern Seas. Marine Biological Association of the United Kingdom, Plymouth, vi + 250 p.Google Scholar
Lentin, J. K. 1985. “Canningia“ turrita Brideaux, 1977, as the lining of a peridinioid calcareous dinoflagellate. American Association of Stratigraphic Palynologists Newsletter, 18(3):8–9.Google Scholar
Levac, E. 2001. High resolution Holocene palynological record from the Scotian Shelf. Marine Micropaleontology, 43:179–197.CrossRefGoogle Scholar
Levac, E. 2003. Palynological records from Bay of Islands, Newfoundland: Direct correlation of Holocene paleoceanographic and climatic changes. Palynology, 27:135–154.Google Scholar
Lewis, J. 1991. Cyst-theca relationships in Scrippsiella (Dinophyceae) and related orthoperidinioid genera. Botanica Marina, 34:91–106.CrossRefGoogle Scholar
Lewis, J. 2002. Data on encystment and excystment rates in dinoflagellates, p. 49–52. In Garcès, E., Zingone, A., Montresor, M., Reguera, B., and Dale, B. (eds.), LIFEHAB: Life Histories of Microalgal Species Causing Harmful Blooms. Research in Enclosed Seas, Series 12, EUR 20361.Google Scholar
Lewis, J., Higman, W. A., and Kuenstner, S. 1995. Occurrence of Alexandrium sp. cysts in sediments from the North East coast of Britain, p. 175–180. In Lassus, P., Arzul, G., Erard-Le Den, E., Gentien, P., and Marcaillou-Le Baut, C. (eds.), Harmful Marine Algal Blooms. Lavoisier Intercept, Paris, France.Google Scholar
Lindemann, E. 1928. Abteilung Peridineae (Dinoflagellatae), p. 3–104. In Engler, A. and Prantl, K. (eds.), Die natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten insbesondere den Nutzpflanzen. Zweite stark vermehrte und verbesserte Auflage herausgegeben von A. Engler. 2. Band. Wilhelm Engelmann, Leipzig.Google Scholar
Loeblich, A. R. III 1976. Dinoflagellate evolution: Speculation and evidence. Journal of Protozoology, 23:13–28.Google Scholar
Loeblich, A. R. III, and Loeblich, L. A. 1979. The systematics of Gonyaulax with special reference to the toxic species, p. 41–46. In Taylor, D. L. and Seliger, H. H. (eds.), Toxic Dinoflagellate Blooms. Elsevier North Holland, New York.Google Scholar
Louwye, S., Head, M. J., and de Schepper, S. 2004. Dinoflagellate cyst stratigraphy and palaeoecology of the Pliocene in northern Belgium, southern North Sea Basin. Geological Magazine, 141:353–378.Google Scholar
Marret, F., and Zonneveld, K. A. F. 2003. Atlas of modern organic-walled dinoflagellate cyst distribution. Review of Palaeobotany and Palynology, 125:1–200.Google Scholar
Matsuoka, K., Kobayashi, S., and Gaines, G. 1990. A new species of the genus Ensiculifera (Dinophyceae): Its cyst and motile form. Bulletin of Plankton Society of Japan, 37:127–143.Google Scholar
McKenzie, C. H., Hatfield, E. A., Harper, F. M., Thompson, R. J., and Parrish, C. C. 1998. Alexandrium fundyense hypnozygote morphology—Implications for encystment and excystment, p. 165–166. In Reguera, B., Blanco, J., Fernández, M. L., and Wyatt, T. (eds.), Harmful Algae. Proceedings of the VIII International Conference on Harmful Algae, Vigo, Spain, 25–29 June 1997. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO.Google Scholar
Medlin, L. K., Lange, M., Wellbrock, U., Donner, G., Elbrächter, M., Hummert, C., and Luckas, B. 1998. Sequence comparisons link toxic European isolates of Alexandrium tamarense from the Orkney Islands to toxic North American stocks. European Journal of Protistology, 34:329–335.Google Scholar
Meier, K. J. S., Janofske, D., and Willems, H. 2002. New calcareous dinoflagellates (Calciodinelloideae) from the Mediterranean Sea. Journal of Phycology, 38:602–615.Google Scholar
Miller, A. A. L., Mudie, P. J., and Scott, D. B. 1982. Holocene history of Bedford Basin, Nova Scotia: Foraminifera, dinoflagellate and pollen records. Canadian Journal of Earth Sciences, 19:2342–2367.Google Scholar
Montresor, M., Janofske, D., and Willems, H. 1997. The cyst-theca relationship in Calciodinellum operosum emend. (Peridiniales, Dinophyceae) and a new approach for the study of calcareous cysts. Journal of Phycology, 33:122–131.CrossRefGoogle Scholar
Montresor, M., Zingone, A., and Marino, D. 1993. The calcareous resting cyst of Pentapharsodinium tyrrhenicum comb. nov. (Dinophyceae). Journal of Phycology, 29:223–230.Google Scholar
Moscatello, S., Rubino, F., Saracino, O. D., Fanelli, G., Belmonte, G., and Boero, F. 2004. Plankton biodiversity around the Salento Peninsula (South East Italy): An integrated water/sediment approach. Scientia Marina, 68(Suppl. 1):85–102.Google Scholar
Mudie, P. J., and Harland, R. 1996. Aquatic Quaternary, p. 843–877. In Jansonius, J. and McGregor, D. C. (eds.), Palynology: Principles and Applications. Vol. 2. American Association of Stratigraphic Palynologists Foundation, Dallas, Texas.Google Scholar
Mudie, P. J., and Short, S. K. 1985. Marine palynology of Baffin Bay, p. 263–308. In Andrews, J. T. (ed.), Quaternary Environments: Eastern Canadian Arctic, Baffin Bay and Western Greenland. George Allen and Unwin, London, United Kingdom.Google Scholar
Mudie, P. J., Rochon, A., and Levac, E. 2002. Palynological records of red tide-producing species in Canada: Past trends and implications for the future. Palaeogeography, Palaeoclimatology, Palaeoecology, 180:159–186.Google Scholar
Nagai, S., Itakura, S., Matsuyama, Y., and Kotani, Y. 2003. Encystment under laboratory conditions of the toxic dinoflagellate Alexandrium tamiyavanichii (Dinophyceae) isolated from the Seto Inland Sea, Japan. Phycologia, 42:646–653.Google Scholar
Nehring, S. 1994. Scrippsiella spp. resting cysts from the German Bight (North Sea): A tool for more complete check-lists of dinoflagellates. Netherlands Journal of Sea Research, 33:57–63.Google Scholar
Nehring, S. 1995. Dinoflagellate resting cysts as factors in phytoplankton ecology of the North Sea. Helgoländer Meeresuntersuchungen, 49:375–392.Google Scholar
Nehring, S. 1997. Dinoflagellate resting cysts from Recent German coastal sediments. Botanica Marina, 40:307–324.Google Scholar
Nuzzo, L., and Montresor, M. 1999. Different excystment patterns in two calcareous cyst-producing species of the dinoflagellate genus Scrippsiella. Journal of Plankton Research, 21:2009–2018.CrossRefGoogle Scholar
Pascher, A. 1914. Über Flagellaten und Algen. Berichte der Deutschen Botanischen Gesellschaft, 36:136–160.Google Scholar
Rochon, A., de Vernal, A., Turon, J.-L., Matthiessen, J., and Head, M. J. 1999. Distribution of recent dinoflagellate cysts in surface sediments from the North Atlantic Ocean and adjacent seas in relation to sea-surface parameters. American Association of Stratigraphic Palynologists Contributions Series, 35:1–152.Google Scholar
Rubino, F., Belmonte, G., Miglietta, A. M., Geraci, S., and Boero, F. 2000. Resting stages of plankton in recent North Adriatic sediments. Marine Ecology, 21:263–284.CrossRefGoogle Scholar
Scholin, C. A. 1998. Morphological, genetic, and biogeographic relationships of the toxic dinoflagellates Alexandrium tamarense, A. catenella, and A. fundyense, p. 13–27. In Anderson, D. M., Cembella, A. D., and Hallegraeff, G. M. (eds.), Physiological Ecology of Harmful Algal Blooms. NATO-Advanced Study Institute Series, G41. Springer-Verlag, Berlin.Google Scholar
Shaw, J., Gareau, P., and Courtney, R. C. 2002. Palaeogeography of Atlantic Canada 13–0 kyr. Quaternary Science Reviews, 21:1861–1878.Google Scholar
Simard, A., and de Vernal, A. 1998. Distribution des kystes du type Alexandrium excavatum dans les sédiments régents et postglaciaires des marges est-Canadiennes. Géographie physique et Quaternaire, 52:361–371.Google Scholar
Solignac, S., de Vernal, A., and Hillaire-Marcel, C. 2004. Holocene sea-surface conditions in the North Atlantic—Contrasted trends and regimes in the western and eastern sectors (Labrador Sea vs. Iceland Basin). Quaternary Science Reviews, 23:319–334.Google Scholar
Steidinger, K. A., and Tangen, K. 1996. Dinoflagellates, p. 387–584. In Tomas, C. R. (ed.), Identifying Marine Diatoms and Dinoflagellates. Academic Press, San Diego.CrossRefGoogle Scholar
Streng, M., Hildebrand-Habel, T., and Willems, H. 2002. Revision of the genera Sphaerodinella Keupp and Versteegh, 1989 and Orthopithonella Keupp in Keupp and Mutterlose, 1984 (Calciodinelloideae, calcareous dinoflagellate cysts). Journal of Paleontology, 76:397–407.Google Scholar
Streng, M., Hildebrand-Habel, T., and Willems, H. 2004. A proposed classification of archeopyle types in calcareous dinoflagellate cysts. Journal of Paleontology, 78:456–483.Google Scholar
Taylor, F. J. R. 1979. The toxigenic gonyaulacoid dinoflagellates, p. 47–56. In Taylor, D. L. and Seliger, H. H. (eds.), Toxic Dinoflagellate Blooms. Elsevier North Holland, New York.Google Scholar
Taylor, F. J. R. 1980. On dinoflagellate evolution. BioSystems, 13:65–108.Google Scholar
Usup, G., Pin, L. C., Ahmad, A., and Teen, L. P. 2002. Phylogenetic relationship of Alexandrium tamiyavanichii (Dinophyceae) to other Alexandrium species based on ribosomal RNA gene sequences. Harmful Algae, 1:59–68.Google Scholar
Verreussel, R. 1997. ‘Spherical cysts.’ Stuifm@il (Newsletter of the Palaeobotanical Palynological Society, Utrecht), 15(3):2–3.Google Scholar
von Stein, F. R. 1883. Der Organismus der Infusionsthiere nach eigenen Forschungen in systematischer Reihenfolge bearbeitet. III. Abteilung. II. Hälfte. Die Naturgeschichte der arthrodelen Flagellaten. Wilhelm Engelmann, Leipzig, 30 p.Google Scholar
Wall, D., and Dale, B. 1968. Quaternary calcareous dinoflagellates (Calciodinellideae) and their natural affinities. Journal of Paleontology, 42:1395–1408.Google Scholar
Wall, D., Guillard, R. R. L., Dale, B., Swift, E., and Watabe, N. 1970. Calcitic resting cysts in Peridinium trochoideum (Stein) Lemmermann, an autotrophic marine dinoflagellate. Phycologia, 9:151–156.CrossRefGoogle Scholar
Watanabe, M. M., Watanabe, M., and Fukuyo, Y. 1982. Encystment and excystment of red tide flagellates. I. Induction of encystment of Scrippsiella trochoidea, p. 27–43. In Eutrophication and red tides in the coastal marine environment—Progress report in 1979–1980; National Institute for Environmental Studies (Japan), Research Report, 30. (In Japanese with English abstract)Google Scholar
Whedon, W. F., and Kofoid, C. A. 1936. Dinoflagellata of the San Francisco region. I. On the skeletal morphology of two new species, Gonyaulax catenella and G. acatenella. University of California Publications in Zoology, 41(4):25–34.Google Scholar
White, A. W., and Lewis, C. M. 1982. Resting cysts of the toxic, red tide dinoflagellate Gonyaulax excavata in Bay of Fundy sediments. Canadian Journal of Fisheries and Aquatic Sciences, 39:1185–1194.Google Scholar
Yamaguchi, M., Itakura, S., Imai, I., and Ishida, Y. 1995. A rapid and precise technique for enumeration of resting cysts of Alexandrium spp. (Dinophyceae) in natural sediments. Phycologia, 34:207–214.Google Scholar
Yoshida, M., Mizushima, K., and Matsuoka, K. 2003. Alexandrium acatenella (Gonyaulacales: Dinophyceae): Morphological characteristics of vegetative cell and resting cyst. Plankton Biology and Ecology, 50:61–64.Google Scholar
Yoshimatsu, S. 1981. Sexual reproduction of Protogonyaulax catenella in culture. 1. Heterothallism. Bulletin of Plankton Society of Japan, 28:131–139. (In Japanese with English abstract)Google Scholar
Zonneveld, K. A. F., Versteegh, G. J. M., de Lange, G. J. 2001. Palaeoproductivity and post-depositional aerobic organic matter decay reflected by dinoflagellate cyst assemblages of the Eastern Mediterranean S1 sapropel. Marine Geology, 172:181–195.Google Scholar