Ensiculifera mexicana, monadoid stage in ventral view, from Li et al. (2020).

Belongs within: Peridiniales.
Contains: Scrippsiella.

The Thoracosphaeraceae are a group of dinoflagellates of which many members are unique among alveolates in producing calcareous structures, either as resting cysts or during vegetative stages (Gottschling et al. 2005, as Calciodinellaceae). Molecular phylogenies also indicate the inclusion of a number of non-calcareous taxa in this clade. Zooxanthella nutricola is a symbiont of radiolarians.

The schizosphere
Published 4 January 2010
Micrographs of Schizosphaerella from Perch-Nielsen (1989).

The dead are all around us. Large parts of the world’s surface are made up by the remains of long-gone marine organisms who left their shells and skeletons, initially constructed for protection from predators and the elements, to form gigantic sedimentary graveyards. Over time, as with everything else, the identities of these unwitting benefactors have changed as new groups supplant the old.

During the Jurassic period, the predominant groups of biomineralising plankton were the calcareous coccoliths and Schizosphaerella (radiolarians were present but only important under certain conditions, planktic foraminiferans would not appear until the Cretaceous, while diatoms appeared in the Jurassic but remained marginalised until during the Cenozoic—Erba 2004). Of these two, Schizosphaerella was particularly significant; at times, it accounted for nearly 100% of plankton-derived carbonate deposition (Mailliot et al. 2007). Schizosphaerella left its remains from the late Triassic to the end of the Jurassic in the form of globular to bell-shaped resting cysts, five to 30 μm in diameter, known as schizospheres. These are composed of two roughly hemispherical plates joined by a simple hinge. The two recognised species, S. punctulata and S. astraea, are distinguished by the presence or absence, respectively, of a subperipheral groove around the hinge and by the lattice arrangement of the elongate radiating elements that make up the wall (Perch-Nielsen 1989). The nature of the Schizosphaerella organism during the active parts of its life cycle (assuming that the fossils are cysts) are unknown, as are its relationships to other organisms. The most common suggestion is that it represents some form of dinoflagellate—calcareous cysts are definitely produced by dinoflagellates of the subfamily Calciodinelloideae. However, Streng et al. (2004) have pointed out that the two-plated hinge arrangement of Schizosphaerella is unlike that known for any dinoflagellate, whose cysts normally open through an archeopyle at one end. That micropalaeontology is littered with examples of taxa of uncertain relationships (becoming more so the further back one goes in time) should come as no surprise to anyone – after all, it is often difficult enough to work out the relationships of modern unicellular organisms on morphological grounds, and doing so is often dependent on features of cell ultrastructure that are unlikely to be preserved in fossils.

Mention should also be made of the nannofossil Stomiosphaera minutissima which was described as having a calcareous cell wall of two layers—a thin inner layer and an outer layer composed of radiating fibres. ‘Stomiosphaera’ was shown by Aubry et al. (1988) to be the same as Schizosphaerella, but diagenetically altered (diagenesis is the process by which the nature of a fossil can be altered by geological processes after it gets deposited). The inner layer represented the two plates of the original fossil fused together while the outer layer resulted from crystal formation around the fossil.

Mean Schizosphaerella size over time compared to levels of carbonate production, from Mattioli et al. (2009).

Schizosphaerella seems to have preferred oligotrophic conditions with a deep nutricline (i.e. nutrients in the sea were spread out rather than being concentrated near the surface). An inverse relationship existed between Schizosphaerella and coccolith abundance (Cobianchi & Picotti 2001) that was also related to the concentration of organic carbon in the water—high organic carbon (i.e. eutrophic conditions) meant more coccoliths and fewer schizospheres, low organic carbon the reverse. Periods of schizosphere abundance also relate to higher sea levels as reduced land level meant reduced organic run-off into the oceans. Both calcareous groups, however, showed reductions during periods of elevated CO2 levels that punctuated the Mesozoic. The Toarcian anoxic event in the early Jurassic seems to have resulted from extensive vulcanism in southern Africa; the mean size of schizospheres becomes much smaller during this period as calcification became reduced by higher ocean acidity (Mattioli et al. 2009). This reduction in calcification is correlated with the extinction of a number of other organisms. Study of such past events is the best means available to us of understanding the effects that elevated carbon dioxide levels could potentially have in our own time (see, palaeontology can be practical too!).

Systematics of Thoracosphaeraceae
Thoracosphaeraceae (see below for synonymy)AS12
    |--+--+--Pernambugia tuberosaGK05
    |  |  `--ScrippsiellaGK05
    |  `--+--+--‘Peridinium’ aciculiferumGK05
    |     |  `--‘Scrippsiella’ hangoeiGK05
    |     `--+--Pfiesteria piscicidaGK05
    |        `--+--Leonella graniferaGK05
    |           `--Thoracosphaera Kamptner 1927GK05, FT93
    |                |--*T. heimii (Lohmann 1920) Kamptner 1944FT93
    |                `--T. imperfecta Kamptner 1946FT93
    `--+--‘Peridinium’ inconspicuumC-SC04
       |--‘Amphidinium’ longumC-SC04
       |--Zooxanthella Brandt 1881C-SC04, FT93 [incl. Philozoon Geddes 1882FT93; Zooxanthellaceae, Zooxanthellales]
       |    `--Z. nutricolaC-SC04
       |--Pentapharsodinium Idelicato & Loeblich 1986GK05, FT93
       |    |--P. daleiGK05
       |    `--P. tyrrhenicumGK05
       `--Ensiculifera Balech 1967GK05, FT93
            |--E. imariensisGK05
            |--E. loeblichii Cox & Arnott 1970GK05
            `--E. mexicana Balech 1967FT93
Thoracosphaeraceae incertae sedis:
  Alasphaera Keupp 1979FT93
    `--A. verrucosaG87
  Calcicarpinum Deflandre 1948FT93
  Calcipterellum Deflandre 1948FT93
  Carinellum Keupp 1981FT93
  Cubodinellum Keupp 1987FT93
  Dimorphosphaera Keupp 1979FT93
  Echinodinella Keupp 1980FT93
  Gonellum Keupp 1987FT93
  Heptasphaera Keupp 1979FT93
  Keuppisphaera Lentin & Williams 1989 [=Hexasphaera Keupp 1987 non Clarke & Verdier 1967]FT93
  Nephrodinella Keupp 1981FT93
  Orthocarinellum Keupp 1987FT93
  Praecalcigonellum Keupp & Versteegh 1989FT93
  Pithonella Lorenz 1902FT93, MS99 (see below for synonymy)
    |--*Cadosinella’ gracillimoides Vogler 1941LT64
    |--P. paratabulataG87
    `--P. patricia-creeleyaeG87
  Sliteria Krasheninnikov & Basov 1983FT93
  Sphaerodinella Keupp & Versteegh 1989FT93
  Tetramerosphaera Willems 1985FT93
  Tetratropis Willems 1990FT93
  Orthopithonella Keupp in Keupp & Mutterlose 1984FT93
    `--O. globosa (Fütterer 1984) Lentin & Williams 1985FT93
  Bicarinellum Deflandre 1948 [incl. Biechelerella Deflandre 1948, Calcisphaerellum Deflandre 1948]FT93
    `--B. calvum Keupp 1979FT93
  Pirumella Bolli 1980 [incl. Obliquipithonella Keupp in Keupp & Mutterlose 1984]FT93
    |--‘Pithonella’ thayeri Bolli 1974 (see below for synonymy)FT93
    |--P. krasheninnikovii (Bolli 1974) Lentin & Williams 1993FM03
    `--‘Obliquipithonella’ patriciagreeleyae (Bölli 1974) Lentin & Williams 1985FT93
  Fibrosphaera Colom 1935MSV00
    `--F. stephanoidea Colom 1935ADD88
  Stomiosphaera Wanner 1940MSV00
    `--*S. moluccana Wanner 1940ADD88
  Cadosina Wanner 1940MSV00
    `--*C. fusca Wanner 1941LT64
  Calcisphaerula Bonet 1956FT93, MSV00
    `--*C. innominata Bonet 1956H75
  Schizosphaerella Deflandre & Dangeard 1938FT93 (see below for synonymy)
    |--*S. punctulata Deflandre & Dangeard 1938 (see below for synonymy)ADD88
    `--S. astraea Moshikovitz 1979 [=S. astrea (l. c.)]ADD88
  Cryptoperidiniopsis brodyiAS12, C-SC04
  Paulsenella Chatton 1920AS12, FT93
  Inocardion Masters & Scott 1978HW93
  Amyloodinium Brown & Hovasse 1946AB19, FT93
    `--A. ocellatumC-SC04
  Blastodinium Chatton 1906AB19, FT93 [Blasinidae, Blastodiniaceae, Blastodinidae, Blastodiniidae]
    |--B. apsteiniCC87
    |--B. chattoniCC87
    |--B. contortumCC87
    |--B. hyalinumCC87
    |--B. pruvotiCC87
    `--B. spinulosum Chatton 1912FT93
  Duboscquodinium Grassé in Chatton 1952AB19, FT93
    |--D. colliniCC87
    `--D. kofoidiCC87

Pithonella Lorenz 1902FT93, MS99 [incl. Cadosinella Vogler 1941FT93, Carpistomiosphaera Nowak 1968FT93, Parastomiosphaera Nowak 1968FT93]

‘Pithonella’ thayeri Bolli 1974 [=Obliquipithonella thayeri (Bolli) Lentin & Williams 1985; incl. *Pirumella edithvincentiae Bolli 1980]FT93

Schizosphaerella Deflandre & Dangeard 1938FT93 [incl. Colomisphaera Nowak 1968ADD88, Nannopatina Stradner 1961ADD88, Nipterula Farinacci 1969ADD88]

*Schizosphaerella punctulata Deflandre & Dangeard 1938 [incl. Nannopatina grandaeva Stradner 1961, Fibrosphaera minutissima Colom 1935 (nom. inv.), Cadosina minutissima, *Colomisphaera minutissima, Stomiosphaera minutissima]ADD88

Thoracosphaeraceae [Cadosinidae, Calciodinellaceae, Calciodinelleae, Calciodinellidae, Calciodinelloideae, Calcisphaerulidae, Obliquipithonelloideae, Orthopithonelleae, Orthopithonelloideae, Pithonellidae, Pithonelloideae, Schizosphaerellaceae, Schizosphaerellidae, Stomiosphaeridae, Thoracosphaerales, Thoracosphaeroideae]AS12

*Type species of generic name indicated


[AB19] Adl, S. M., D. Bass, C. E. Lane, J. Lukeš, C. L. Schoch, A. Smirnov, S. Agatha, C. Berney, M. W. Brown, F. Burki, P. Cárdenas, I. Čepička, L. Chistyakova, J. del Campo, M. Dunthorn, B. Edvardsen, Y. Eglit, L. Guillou, V. Hampl, A. A. Heiss, M. Hoppenrath, T. Y. James, A. Karnkowska, S. Karpov, E. Kim, M. Kolisko, A. Kudryavtsev, D. J. G. Lahr, E. Lara, L. Le Gall, D. H. Lynn, D. G. Mann, R. Massana, E. A. D. Mitchell, C. Morrow, J. S. Park, J. W. Pawlowski, M. J. Powell, D. J. Richter, S. Rueckert, L. Shadwick, S. Shimano, F. W. Spiegel, G. Torruella, N. Youssef, V. Zlatogursky & Q. Zhang. 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66: 4–119.

[AS12] Adl, S. M., A. G. B. Simpson, C. E. Lane, J. Lukeš, D. Bass, S. S. Bowser, M. W. Brown, F. Burki, M. Dunthorn, V. Hampl, A. Heiss, M. Hoppenrath, E. Lara, E. Le Gall, D. H. Lynn, H. McManus, E. A. D. Mitchell, S. E. Mozley-Stanridge, L. W. Parfrey, J. Pawlowski, S. Rueckert, L. Shadwick, C. L. Schoch, A. Smirnov & F. W. Spiegel. 2012. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59 (5): 429–493.

[ADD88] Aubry, M.-P., F. Depêche & T. Dufour. 1988. Stomiosphaera minutissima (Colom, 1935) from the Lias of Mallorca (Balearic Islands) and Umbria (Italy), and Schizosphaerella punctulata Deflandre & Dangeard, 1938: taxonomic revision. Geobios 21 (6): 709–727.

[CC87] Cachon, J., & M. Cachon. 1987. Parasitic dinoflagellates. In: Taylor, F. J. R. (ed.) The Biology of Dinoflagellates pp. 571–610. Blackwell Scientific.

[C-SC04] Cavalier-Smith, T., & E. E. Chao. 2004. Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.) European Journal of Protistology 40: 185–212.

Cobianchi, M., & V. Picotti. 2001. Sedimentary and biological response to sea-level and palaeoceanographic changes of a Lower–Middle Jurassic Tethyan platform margin (Southern Alps, Italy). Palaeogeography, Palaeoclimatology, Palaeoecology 169 (3–4): 219–244.

Erba, E. 2004. Calcareous nannofossils and Mesozoic oceanic anoxic events. Marine Micropaleontology 52: 85–106.

[FT93] Fensome, R. A., F. J. R. Taylor, G. Norris, W. A. S. Sarjeant, D. I. Wharton & G. L. Williams. 1993. A classification of living and fossil dinoflagellates. Micropaleontology Special Publication 7: i–viii, 1–351.

[FM03] Friedrich, O., & K. J. S. Meier. 2003. Stable isotope indication for the cyst formation depth of Campanian/Maastrichtian calcareous dinoflagellates. Micropaleontology 49 (4): 375–380.

[G87] Goodman, D. K. 1987. Dinoflagellate cysts in ancient and modern sediments. In: Taylor, F. J. R. (ed.) The Biology of Dinoflagellates pp. 649–722. Blackwell Scientific.

[GK05] Gottschling, M., H. Keupp, J. Plötner, R. Knop, H. Willems & M. Kirsch. 2005. Phylogeny of calcareous dinoflagellates as inferred from ITS and ribosomal sequence data. Molecular Phylogenetics and Evolution 36: 444–455.

[H75] Häntzschel, W. 1975. Treatise on Invertebrate Paleontology pt W. Miscellanea Suppl. 1. Trace Fossils and Problematica 2nd ed. The Geological Society of America: Boulder (Colorado), and The University of Kansas: Lawrence (Kansas).

[HW93] Hart, M. B., & C. L. Williams. 1993. Protozoa. In: Benton, M. J. (ed.) The Fossil Record 2 pp. 43–70. Chapman & Hall: London.

[LT64] Loeblich, A. R., Jr & H. Tappan. 1964. Sarcodina: chiefly “thecamoebians” and Foraminiferida. In Moore, R. C. (ed.) Treatise on Invertebrate Paleontology pt C. Protista 2 vol. 2. The Geological Society of America and The University of Kansas Press.

Mailliot, S., S. Elmi, E. Mattioli & B. Pittet. 2007. Calcareous nannofossil assemblages across the Pliensbachian/Toarcian boundary at the Peniche section (Ponta do Trovão, Lusitanian Basin). Ciencias da Terra (UNL) 16: 1–13.

Mattioli, E., B. Pittet, L. Petitpierre & S. Mailliot. 2009. Dramatic decrease of pelagic carbonate production by nannoplankton across the Early Toarcian anoxic event (T-OAE). Global and Planetary Change 65 (3-4): 134–145.

[MS99] Munnecke, A., C. Samtleben, T. Servais & D. Vachard. 1999. SEM-observation of calcareous micro- and nannofossils incertae sedis from the Silurian of Gotland, Sweden: preliminary results. Geobios 32 (2): 307–314.

[MSV00] Munnecke, A., T. Servais & D. Vachard. 2000. A new family of calcareous microfossils from the Silurian of Gotland, Sweden. Palaeontology 43 (6): 1153–1172.

Perch-Nielsen, K. 1989. Mesozoic calcareous nannofossils. In: Bolli, H. M., J. B. Saunders & K. Perch-Nielsen (eds) Plankton Stratigraphy vol. 1. Planktic foraminifera, calcareous nannofossils and calpionellids pp. 329–426. Cambridge University Press.

Streng, M., T. Hildebrand-Habel & H. Willems. 2004. A proposed classification of archeopyle types in calcareous dinoflagellate cysts. Journal of Paleontology 78 (3): 456–483.

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