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Neoceratium Gen. Nov., a New Genus for All Marine Species Currently Assigned to Ceratium (Dinophyceae)

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Neoceratium Gen. Nov., a New Genus for All Marine Species Currently Assigned to Ceratium (Dinophyceae) ARTICLE IN PRESS Protist, Vol. ], ]]]–]]], ]] ]]]] http://www.elsevier.de/protis Published online date 10 August 2009 ORIGINAL PAPER Neoceratium gen. nov., a New Genus for All Marine Species Currently Assigned to Ceratium (Dinophyceae) Fernando Gomez´ a,1, David Moreirab, and Purificacion´ Lopez-Garc´ ıa´ b aObservatoire Oceanologique de Banyuls sur Mer, Universite Pierre et Marie Curie, CNRS UMR 7621, Avenue du Fontaule, BP 44, F-66651 Banyuls sur Mer, France bUnite d’Ecologie, Systematique et Evolution, CNRS UMR 8079, Universite Paris-Sud, Batimentˆ 360, 91405 Orsay Cedex, France Submitted October 23, 2008; Accepted June 13, 2009 Monitoring Editor: Marina Montresor The dinoflagellate genus Ceratium contains marine and freshwater species. Freshwater species possess six cingular plates, thick plates in the concave ventral area and usually develop a third hypothecal horn. The marine Ceratium species (462 species) possess five cingular plates and thin plates in the concave ventral area; a third hypothecal horn is atypical. Resting cysts, a common feature in the freshwater species, are unreported in marine species. We illustrate for the first time resting cysts in marine Ceratium species (C. furca and C. candelabrum). We obtained small subunit ribosomal RNA gene (SSU rDNA) sequences of 23 Ceratium species (more than one third of the total marine species described so far), with representatives of the four acknowledged subgenera. Phylogenetic analyses including the type species, the freshwater C. hirundinella, showed that the four available sequences of freshwater species formed a strongly supported subclade, very distant from the marine cluster. Our data support the splitting of Ceratium sensu lato into two genera. Ceratium sensu stricto should be reserved for freshwater species possessing six cingular plates (three cingular plates in dorsal view). The new genus name, Neoceratium gen. nov. should be applied to the marine species of Ceratium sensu lato that possess five cingular plates (two cingular plates in dorsal view). & 2009 Elsevier GmbH. All rights reserved. Key words: alveolate evolution; Dinoflagellata; Neoceratium gen. nov.; new combination; resting cyst; SSU rDNA phylogeny. Introduction The genus Ceratium Schrank is the earliest genus easy to collect, while the tough theca ensures name in use for a dinoflagellate (Schrank 1793) that morphological features essential for taxo- and is one of the most important phytoplankton nomic analysis are preserved. The genus contains components. The large cell size of Ceratium species, mainly 100-300 mm long, make them Abbreviations: PCR, Polymerase chain reaction; SSU, small subunit; GPP complex (Gymnodiniales, 1Corresponding author; fax +33 468887398 Peridiniales, Prorocentrales) complex; rDNA, ribo- e-mail fernando.gomez@fitoplancton.com (F. Gomez).´ somal deoxyribonucleic acid & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.protis.2009.06.004 Please cite this article as: Gomez´ F, et al. Neoceratium gen. nov., a New Genus for All Marine Species Currently Assigned to Ceratium (Dinophyceae), Protist (2009), doi:10.1016/j.protis.2009.06.004 ARTICLE IN PRESS 2 F. G omez´ et al. a large number of species that are truly planktonic tabulation as a criterion for species diagnosis. and widely distributed in all seas and epiconti- Vanhoffen’s¨ genera were ranked as subgenera: nental waters. More than 120 marine species and Amphiceratium (Vanhoffen)¨ Ostenfeld (Ostenfeld infraspecies, varieties or forms, have been 1903; Paulsen 1908), Biceratium (Vanhoffen)¨ described and about 62 out of them are con- Ostenfeld (Ostenfeld 1903; Paulsen 1908), sidered valid (Gomez´ 2005). Only four species, Archaeceratium Jørgensen ((Jørgensen 1911) with numerous varieties, have colonized epiconti- =Poroceratium (Vanhoffen)¨ Pavillard (Pavillard nental waters (Popovsky and Pfiester 1990 1916)) and Ceratium sensu stricto was named Popovsky and Pfiester 1990). Tripoceratium Kofoid (Kofoid 1909,=Euceratium The first illustrations of Ceratium appeared in (Gran) Ostenfeld (Gran 1902; Ostenfeld 1903), the classic work of O.F. Muller¨ (1786) that =Orthoceratium Sournia (Sournia 1968)). Each described one freshwater and one marine species subgenus was further divided into sections and as Bursaria hirundinella O.F. Muller¨ and Cercaria subsections based on the cell contour similarities tripos O.F. Muller,¨ respectively. Under these gen- (Bohm¨ 1931; Gran 1902; Jørgensen 1911, 1920; era, O.F. Muller¨ described also other organisms Karsten 1907; Kofoid 1909; Ostenfeld 1903; that were not related to dinoflagellates (Muller¨ Paulsen 1908; Pavillard 1907). The freshwater 1786). Schrank (1793, 1802) created the genus species of Ceratium (section Cornuta) were placed Ceratium for the species C. pleuroceras, C. in the subgenus Biceratium (Jørgensen 1911; tetraceras and later C. macroceras from material Schiller 1937; Sournia 1968). collected in a lake in central Europe. Nitzsch The subgenus Tripoceratium exhibits the classi- (1817) realized that Cercaria tripos O.F. Muller¨ cal ‘anchor’ shape in which both antapical horns belonged to Schrank’s genus and made the proceed laterally after leaving the body (e.g. C. transfer into Ceratium. Marine and freshwater tripos). Biceratium includes species characterized species of Ceratium described thereafter were by a distinct apical horn and unequal antapical placed under Schrank’s genus. Bursaria hirundi- horns that are directed posteriorly (e.g. C. furca). nella O.F. Muller¨ was also transferred into Cer- Archaeceratium was created for a few rare atium (Dujardin 1841). The specimens described species that have a high flattened apical horn by Schrank (1793) - i.e. C. pleuroceras, C. (e.g. C. gravidum). The subgenus Amphiceratium tetraceras and C. macroceras - corresponded to (contains a few elongated species with both Bursaria hirundinella and consequently they are hypothecal horns directed posteriorly. The right regarded as synonyms of C. hirundinella (O.F. horn is greatly reduced and the left one is often Muller)¨ Dujardin (Popovski and Pfiester 1990). very extended (e.g. C. fusus). However, the name of the type species of the The morphology of the freshwater and marine genus Ceratium has to be designed from the Ceratium species has been investigated in detail Schrank’s species epithet: C. pleuroceras or C. with optical (Bourrelly 1968; Entz 1927), and tetraceras. Loeblich Jr and Loeblich III (1966) transmission and scanning electron microscopy considered C. pleuroceras, the first of the species (Dodge and Crawford 1970; Wetherbee 1975). In mentioned by Schrank (1793), as the type species older literature, the nomenclature of the thecal of the genus. However, the International Code of plates varies among authors, until Kofoid (1907a) Botanical Nomenclature (Farr et al. 1979) gave the proposed a new system of tabulation that was priority to the lectotypification of C. tetraceras, the widely accepted. After the analysis of seventeen second species cited by Schrank, by Dujardin marine species, Kofoid (1907a) concluded that (1841). Ceratium have four apical (40), four precingular Vanhoffen¨ (1896) questioned the unity of the (400), four cingular (4c), five postcingular (5000) and genus Ceratium and proposed its split into four two antapical (20000) plates. Kofoid (1907a) did not genera based on the shape of the cell body and investigate the plates of the concave ventral area horns: Amphiceratium, Biceratium, Poroceratium, that are highly delicate in the marine species and and Ceratium sensu stricto. Kofoid (1907a) stu- he erroneously considered four precingular plates died the tabulation of seventeen marine species (400) instead of five (500). The plates of the concave with representatives of each subgenus. He ventral area are more robust in the freshwater demonstrated the unity of the tabulation within species and Entz (1927, p. 350) illustrated that this the genus and rejected the split of Ceratium into area was composed of three large plates (X, Y, Z) four genera proposed by Vanhoffen.¨ This drove plus several sulcal platelets. He considered the further studies of Ceratium towards the analysis of plate X as the sixth precingular plate. Entz (1927) the silhouettes and ornamentation rather than the did not illustrate the cingular plates. Bourrelly Please cite this article as: Gomez´ F, et al. Neoceratium gen. nov., a New Genus for All Marine Species Currently Assigned to Ceratium (Dinophyceae), Protist (2009), doi:10.1016/j.protis.2009.06.004 ARTICLE IN PRESS Neoceratium, New Genus for Marine Ceratium Species 3 (1968) examined three freshwater species and Ceratium and obtained strong support for the observed five cingular plates, whereas the marine separation of freshwater and marine species into species had only four (Kofoid had not examined two different genera. In addition to the phylogeny any freshwater species when he proposed the results, our observations allowed us to discuss the tabulational unity of Ceratium in 1907). The validity of some morphological characters that are dinoflagellate cingular and hypothecal plates are used for the diagnostic separation between considered more conservative and stable taxono- marine and freshwater species. For example, mical characters than those of the epitheca although resting cysts are common in freshwater (Balech 1980). Nevertheless, the split of the genus species but were unknown from marine ones, we based on the different number of cingular plates in report their existence in at least two marine marine and freshwater species has been a matter
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