Plate Pattern Clarification of the Marine Dinophyte Heterocapsa Triquetra Sensu Stein (Dinophyceae) Collected at the Kiel Fjord (Germany)1

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Plate Pattern Clarification of the Marine Dinophyte Heterocapsa Triquetra Sensu Stein (Dinophyceae) Collected at the Kiel Fjord (Germany)1 J. Phycol. 53, 1305–1324 (2017) © 2017 Phycological Society of America DOI: 10.1111/jpy.12584 PLATE PATTERN CLARIFICATION OF THE MARINE DINOPHYTE HETEROCAPSA TRIQUETRA SENSU STEIN (DINOPHYCEAE) COLLECTED AT THE KIEL FJORD (GERMANY)1 Urban Tillmann 2 Alfred Wegener Institut, Helmholz-Zentrum fur€ Polar- und Meeresforschung, Am Handelshafen 12, D – 27570, Bremerhaven, Germany Mona Hoppenrath2 Senckenberg am Meer, German Centre for Marine Biodiversity Research (DZMB), Sudstrand€ 44, D – 26382, Wilhelmshaven, Germany Marc Gottschling Department Biologie, Systematische Botanik und Mykologie, GeoBio-Center, Ludwig-Maximilians-Universit€at Munchen,€ Menzinger Str. 67, D – 80638, Munchen,€ Germany Wolf-Henning Kusber Botanischer Garten und Botanisches Museum Berlin-Dahlem, Freie Universit€at Berlin, Konigin-Luise-Straße€ 6-8, D – 14195, Berlin, Germany and Malte Elbrachter€ Wattenmeerstation Sylt des Alfred-Wegener-Institut, Helmholtz-Zentrum fur€ Polar- und Meeresforschung, Hafenstr. 43, D – 25992, List/Sylt, Germany One of the most common marine dinophytes is a 254–306 nm in diameter, had 6 ridges radiating from species known as Heterocapsa triquetra.WhenStein a central spine, 9 peripheral and 3 radiating spines, introduced the taxon Heterocapsa, he formally based and 12 peripheral bars as well as a central depression the type species H. triquetra on the basionym in the basal plate. Our work provides a clarification Glenodinium triquetrum. The latter was described by of morphological characters and a new, validly Ehrenberg and is most likely a species of published name for this important but yet formally Kryptoperidinium. In addition to that currently undescribed species of Heterocapsa: H. steinii sp. nov. unresolved nomenclatural situation, the thecal plate Key index words: H. triquetra morphology; plate pattern; taxon- composition of sensu Stein (1883) was omy; variability controversial in the past. To clarify the debate, we collected material and established the strain UTKG7 Abbreviations: APC, apical pore complex; BPP, from the Baltic Sea off Kiel (Germany, the same Bayesian posterior probabilities; C, cingular plate; locality as Stein had studied), which was investigated cp, cover plate; GTR, generalized time reversible; using light and electron microscopy, and whose HMDS, hexamethyldisilazane; ICN, International systematic position was inferred using molecular code of nomenclature for algae, fungi, and plants; phylogenetics. The small motile cells (18–26 lmin LBS, Maximum Likelihood bootstrap support; LF, length) had a biconical through fusiform shape and longitudinal flagellum; ML, Maximum Likelihood; typically were characterized by a short asymmetrically OTU, operational taxonomic unit; Po, pore plate; shaped, horn-like protuberance at the antapex. A Sa, anterior sulcal plate; Sd, right sulcal plate; Sp, large spherical nucleus was located in the episome, posterior sulcal plate; Ssa, anterior left sulcal plate; whereas a single pyrenoid laid in the lower cingular Ssp, posterior left sulcal plate; TF, transverse flagel- plane. The predominant plate pattern was identified lum; X, canal-plate as apical pore complex (Po, cp?, X), 40,2a,600,6c, 5s, 5000,20000. The triradiate body scales were About 20 species have been assigned to dino- phycean Heterocapsa (Iwataki 2008, Guiry 2017) 1Received 10 May 2017. Accepted 29 August 2017. First Published including cosmopolitan bloom formers such as H. ro- Online 15 September 2017. Published Online 10 October 2017, Wiley tundata (Hansen 1989) and the toxic H. circula- Online Library (wileyonlinelibrary.com). risquama (Nagai et al. 1996). The latter has caused 2Authors for correspondence: e-mail [email protected] and [email protected]. severe bivalve mortalities in Japan in 1992 (Mat- Editorial Responsibility: T. Mock (Associate Editor) suyama et al. 1997) and since then, it is a serious 1305 1306 URBANTILLMANNETAL. threat to the mussel industry in western Japan and plate as belonging to the precingular series. Based on Hong Kong (Iwataki et al. 2002). Another species, cur- Lindemann (1924) and Lebour (1925), Schiller rently known as Heterocapsa triquetra, is one of the most (1937) thus registered somewhat indecisively the plate abundant bloom-forming dinophyte species in coastal pattern of H. triquetra sensu Stein (1883) as [sic] 40, and estuarine waters, with a wide distribution around 2a, 700,(600), 5000,20000 in his seminal pre-war book. the world (Carstensen et al. 2015). It is regularly The next important addition came in 1977 when, recorded from the North Sea, the Baltic Sea, the for the first time, Pennick and Clarke (1977) described North and South Atlantic, along the west and east the presence of three-dimensional body scales for coast of Greenland, the Mediterranean and in the east- H. triquetra sensu Stein (1883). Subsequently, Morrill ern Pacific (Lohmann 1908, Lebour 1925, Braarud and Loeblich (1981) detected similar scales in two spe- 1935, Grontved and Seidenfaden 1938, Braarud and cies assigned to Cachonina. These scales are unique in Pappas 1951, Balech 1988). Dense blooming popula- their three-dimensional architecture, which led Morrill tions frequently occur in estuaries and harbor areas, and Loeblich (1981) to aim at the comparison of the but are also recorded from a brackish lake below thick plate patterns in H. triquetra sensu Stein (1883) and in surface ice (Baek et al. 2011). Typical bloom densities species assigned to Cachonina. Based on cultivated À range from 1–20 9 106 cells Á L 1 (Lindholm and material they reported a large variability regarding the Nummelin 1999, Litaker et al. 2002a, Tas 2016). Fur- number of plates and described the “most common” ther studies of H. triquetra sensu Stein (1883) comprise plate formula of H. triquetra sensu Stein (1883) as a wide array of investigations in ecophysiology having2pr,50,3a,700, 6c, 7s, 5000,1p,20000 (whereas “pr” (Braarud and Pappas 1951, Litaker et al. 2002b), fatty refers to preapical plates; i.e., a pore plate Po and a acid composition (Matsuyama and Suzuki 1998), canal plate X). This plate pattern notably consists of phagotrophy (Legrand et al. 1998), life-history (Olli one additional plate in each of the three epithecal 2004), vertical migration (Jephson et al. 2011), phylo- plate series in comparison to the results of Lindemann genetics (Salas et al. 2014, Price and Bhattacharya (1924). However, the discrepancy was not even men- 2017), and entire genome assessment (McEwan et al. tioned by Morrill and Loeblich (1981). Their plate pat- 2008). tern determined for H. triquetra sensu Stein (1883) in Heterocapsa triquetra sensu Stein (1883) is thus one fact is congruent to that of Cachonina (Loeblich 1968), of the most frequently encountered and best studied and this congruence, together with the presence of marine representatives of unicellular dinophytes. It is the characteristic body scales, was the reasons to bring relatively small (ca. 16–30 lm long, 9–18 lm wide) Cachonina into synonymy with Heterocapsa (Morrill and but characteristic because of its unique fusiform Loeblich 1981). shape. Furthermore, the horn-like hypothecal protu- Seven years later, Balech (1988) published thecal berance is a highly diagnostic trait making the recog- plates of H. triquetra sensu Stein (1883) in detail nition and identification of the species exceptionally based on material of South Atlantic origin. It easy despite its small size. In the initial descriptions remains unclear whether Balech (1988) was not and minute illustrations, Stein (1883) referred to the- aware of, or whether his practical work preceded cal plates (and sutures between them) of the epitheca the study of, Morrill and Loeblich (1981). In any only. In fact, he regarded this hemispheric tabulation case, his work using field samples basically con- as the main difference between his new Heterocapsa firmed the results of Lindemann (1924) for the con- and other thecate taxa recognized during his time, formation of epi- and hypothecal plates. Additional such as Peridinium (plates visible in light microscopy: work on cingular and sulcal plates led Balech LM) and Glenodinium (plates not visible in LM). (1988) to conclude the complete plate formula as Heterocapsa triquetra sensu Stein (1883) became Po, 40, 2a, 700, 6c, 4s, 5000,20000. As Lebour (1925), established fast (Butschli€ 1885, Schutt€ 1895, Delage Balech (1988) considered the plate in the midven- and Herouard 1896, Lohmann 1908, Paulsen 1908, tral area as plate number 7 of the precingular series, Meunier 1910, 1919). Schutt€ (1895) was the first who whereas Lindemann (1924) regarded this area as observed and depicted plates of the hypotheca, and part of the cingular and sulcal groove system. The was followed by Meunier (1919) showing hypothecal latest revision of plate patterns goes back to the revi- plates in ventral and dorsal views. Lindemann (1924) sionary work of Iwataki (2002), who concluded the re-examined Stein’s species based on plankton mate- same plate pattern for all species of Heterocapsa, rial from the Mediterranean Golden Horn, as well as including H. triquetra sensu Stein (1883), namely from the Baltic Sea off Kiel and Rostock, and pre- Po, X, 50, 3a, 700, 6c, 5s, 5000,20000. Thus, the emenda- sented the complete tabulation pattern of both epi- tion of Heterocapsa (Iwataki et al. 2003) is in conflict and hypotheca for the first time in detail. He did not with the delicate work of Lindemann (1924), resolve cingular and sulcal plates, but his descriptions Lebour (1925) and Balech (1988).
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