An Unnoticed Dinoflagellate in the Pacific Ocean 15

Phycological Research 2004; 52: 13–16

Research note New records of Scaphodinium mirabile (Dinophyceae), an unnoticed dinoﬂagellate in the Paciﬁc Ocean

Fernando Gómez* and Ken Furuya Department of Aquatic Biosciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113–8657, Japan

shaped, encapsulated nucleus. No chloroplasts are SUMMARY present and the cytoplasm contains a uniform network of myo-fibrils (Cachon and Cachon 1969; Sournia 1986). Previous records of dinoflagellate Scaphodinium mira- The type species of this monotypic genus, Scaphod- bile Margalef (Leptodiscaceae, Noctilucales) were inium mirabile Margalef, was originally described from restricted to the Mediterranean-Black Sea and Eastern the Spanish Mediterranean coastal waters (Margalef Atlantic Ocean. Nine and 34 specimens were observed 1963). From the NW Mediterranean Sea, Cachon and in the upper 100 m layer in May and July, respectively, Cachon-Enjumet (1964) reported the taxonomic junior in a cross-section in the vicinity of the Kuroshio Current synonym Leptospathium navicula. The species has been (NW Pacific Ocean). Nearly all the Lugol-fixed speci- further reported in the Mediterranean Sea (Margalef mens appeared folded over themselves, an appearance 1969a,b; Léger 1971; Abboud-Abi Saab 1989; Gómez that differs from the view reported in the scarce and Gorsky 2003), the Eastern Atlantic Ocean Margalef literature available. (1973, 1975) and recently from the Marmara and Black Seas (Balkis 2000; Stoyanova 1999). Key words: aberrant dinoflagellate, Dinophyceae, Dino- This study reports for the first time Scaphodinium phyta, Kuroshio Current, Noctilucales, Pacific Ocean, mirabile in the Pacific Ocean. Notes on the distribu- phytoplankton, Scaphodinium, taxonomy. tion, morphology, and on the reasons for the apparent underestimation of this species are given below. The role of heterotrophic and mixotrophic phytoplank- The material was collected from two cruises (13–20 ton, in particular dinoflagellates, on pelagic food webs May and 3–10 July, 2002) aboard R/V Soyo-maru has recently received significant attention (Gaines and carried out along the meridian 138° in the vicinity of Elbrächter 1987; Hansen 1991). However, among the Kuroshio Current. During the cruise in May, nine heterotrophic dinoflagellates, taxa belonging to the stations were sampled from 30°30′N to 34°15′N. In order Noctilucales Haeckel (see Gómez 2003 for a July 10 stations were sampled from 30°0′N to 34°20′N. species list) have received less attention, with the At each station, 15 discrete depths from 5–200 m exception of the red tide species Noctiluca scintillans were sampled with Niskin bottles (Table 1). Seawater (Macartney) Kofoid. samples were preserved with acidified Lugol’s solution The morphology of the Noctilucales differs markedly (Hasle and Syvertsen 1997; p. 334) and stored at about from the Peridiniales, notably by the presence of 5°C. Samples were preconcentrated via settling in glass contractile muscle-like fibrils involved in movements cylinders, and concentrates settled in standard sedi- and cell shape changes (Cachon and Cachon-Enjumet mentation chambers. Concentrates equivalent to 400 mL 1964, 1966; Cachon and Cachon 1967a,b, 1969). were observed with a Nikon inverted microscope equipped Members of the family Leptodiscaceae F.J.R. Taylor are with a Nikon digital camera. One specimen in the volume strongly flattened antero-posteriorly and display a wing- examined (1 cell/0.4 L) corresponds to 2.5 cells L–1. like extension (the velum) not associated with either The number of samples analyzed was 131 in May the cingulum or the sulcus (Taylor 1976; p. 184; Fensome and 144 in July, representing a total volume of 106 L et al. 1993; p. 182; regarding the authorship of the of seawater examined in both cruises. In May nine family Leptodiscaceae see Fensome et al. 1993; p. 183). specimens of Scaphodinium were found in eight samples Scaphodinium is an extremely flattened biflagellate (6% of the total samples), whereas in July, 34 specimens cell, usually folded over one of its faces. The flattened portion is projected in both ends, with the extension closest to the nucleus being bilobulate, shorter and *To whom correspondence should be addressed. wider than the other. No sulcus or cingulum have been Email: [email protected] reported; the proximal parts of both flagella are sheathed Communicating editor: G. Hansen. in tube-like channels located next to the large, egg- Received 25 April 2003; accepted 12 August 2003.

14 F. Gómez and K. Furuya

′ were found in 29 samples (20% of the total samples). 0 ° The maximum number of specimens found in a single B01 30 sample (0.4 L) was three (Table 1). Nearly all the

′ specimens were recorded in the upper 100 m layer. 30 ° The number of records was higher in the summer than C02 30 in the spring (Table 1). ′

0 The morphology of leptodiscaceans results in a °

C03 difficult interpretation of cell orientation. According to 31 the interpretation by Cachon and Cachon (1969) the ′

30 part of the cell containing the flagella is considered the °

C04 hyposoma. During routine microscopical observation, 31 the specimens appeared in several views with different ′ 0

° appearances (Figs 1–4,6–12). The non-folded view found C05 32 in the literature (Sournia 1986; fig. 143) was only ′ July found in two of 43 specimens observed (Figs 1,2). The 30

° flagella were not visible in most specimens, probably C06 32 because they were lost as a result of the fixation. The

′ transverse flagellum (TF), as defined by Cachon and 0 °

C07 Cachon (1969), is usually coil-shaped and larger than 33 the longitudinal flagellum (Figs 2,3,8–10). The inser- ′ tion of the TF is located between the nucleus and the 30 °

C08 bi-lobuled extremity (Figs 3,7). Fensome et al. (1993; 33

E p. 182) apparently followed the interpretation of the ′ °

45 orientation by Cachon and Cachon (1969). However ° B02

33 the orientation of the cell and the labeling of the

′ flagella by Fensome et al. (1993; their fig. 186D) is 15

° the reverse of Cachon and Cachon (1969) interpreta- B03

34 tion and even the path of each flagellum is different. Nearly all the Lugol-fixed specimens appeared ′ folded, extremity against extremity (Figs 3,4,6–10). In 30 °

C13 lateral views, considered here as the view showing the 30 extreme low thickness in relation to the cell body, the ′

0 flagella appeared to the exterior side (Figs 3,6–10). ° C12

31 One of the specimens observed was undergoing binary

′ fission (Figs 11,12).

30 Scaphodinium can be considered homogeneously ° C11

31 distributed in the euphotic zone, with no clear latitudi-

′ nal trends, despite the studied area covering a wide 0 ° range of hydrographical and trophic conditions. It can C10 32

collected at each sample (0.4 L) along the meridian 138 only be inferred that this taxon tends to be more

′ abundant in the summer (Table 1). In the Black Sea, 30 May ° this species was also more common during the summer C09 32 (Stoyanova 1999). The salinity does not seem to ′

0 influence on the distribution of Scaphodinium, if it is °

C06 taken into account the wide range of salinity where the 33 species has been recorded, from the saline waters of ′ Scaphodinium mirabile

30 the eastern Mediterranean basin (salinity of 38–39) to ° C03

33 the brackish waters of the Black Sea with salinity values of 15–18 (Stoyanova 1999). Concerning the ′ 0

° trophic conditions, the eutrophic Black Sea waters B01 33 strongly differ from the oligotrophy that prevails in the

′ adjacent waters of the Kuroshio Current. 20 00000000 0 1110100000 00000001 000000000 0011000100 000100000 0000000000 000000000 000000000– 000000000 100000––0– – 0000000000 ° Despite its relatively large size, which renders the C01 34

Number of specimens organisms easily collectable by net or bottle sampling, records of Scaphodinium are scarce. Other reasons for the underestimation of Scaphodinium, during routine 10000 0 0000001000 – 0 1100301000 00000–000– 0 0000000111 0 0000100000 0–1000000000 0221000200 0–200–01–000 0000010011 0–3000000000 1010000100 0–4000010000 0001100000 –5000000000 –6000000000 –7002000000 –8000001001 –9000000001 Table 1. Table Depth: –5 –100 –125 –150 –175 –200 Station Latitude analyses are:

An unnoticed dinoflagellate in the Pacific Ocean 15

Figs 1–12. Photomicrographs of Scaphodinium mirabile Margalef and (Fig. 5) of an appendicularian. 1,2. A non-folded specimen with a coil-shape transverse flagellum (TF). Scale bar = 100 µm (May St. 9, 80 m depth). 3,4. Two views of the same specimen. The arrow points at the insertion of the TF (July B02, 60 m depth). 5. An appendicularian here presented for a comparison to the lateral views of Scaphodinium. 6,7. Lateral views of a specimen showing the longitudinal (LF) and transverse flagella (July St. 3, 40 m depth). 8–10. Several views of the same specimen showing the TF (May St. 6, 20 m depth). 11,12. Two views of a specimen under division (July St. 6, 5 m depth).

16 F. Gómez and K. Furuya

1 Scaphodinium is usually missing in the literature gen. sp., péridiniens Noctilucidae (Hertwig) du plancton used for phytoplankton identification, with the excep- néritique de Villefranche-sur-Mer. Bull. Inst Océanogr. tion of Sournia (1986) and Fensome et al. (1993). Monaco 62: 1–12. The original description of the species (Margalef Cachon, J. and Cachon-Enjumet, M. 1966. Pomatodinium 1963) and further records (Cachon and Cachon- impatiens nov. gen. nov. sp. péridiniens Noctilucidae Enjumet 1964; Margalef 1969a,b, 1973, 1975; Kent. Protistologica 2: 23–30. Léger 1971; Abboud-Abi Saab 1989; Stoyanova Fensome, R. A., Taylor, F. J. R, Norris, G., Sarjeant, W. A. S., 1999; Balkis 2000) appeared in journals that are Wharton, D. I. and Williams, G. L. 1993. A classification not easily accessible. of living and fossil dinoflagellates. J. Micropaleontology 7: 2 The morphology of leptodiscaceans is highly modi- (special publication) 1–351. fied compared to typical dinoflagellates (Peridini- Gaines, G. and Elbrächter, M. 1987. Heterotrophic nutrition. ales). The lack of a cingulum, sulcus and the possible In Taylor, F. J. R. (Ed.) The Biology of Dinoflagellates. loss of the flagella by fixation, contribute to the Botanical Monographs, Vol. 21. Blackwell Science, Oxford, difficulties in identification. In the microscope, pp. 224–68. Lugol-fixed cells of Scaphodinium appear in views Gómez, F. 2003. Checklist of Mediterranean free-living dino- with different appearances that only with difficulty flagellates. Bot. Mar. 46: 215–242. can be considered as a dinoflagellate (Figs 1–4,6–10). Gómez, F. and Gorsky, G. 2003. Microplankton annual cycles 3 The photomicrographs or drawings reported in the in the Bay of Villefranche, Ligurian Sea, NW Mediterra- literature show views of non-folded cells. However, nean. J. Plank. Res. 25: 323–39. in this study nearly all Lugol-fixed specimens were Hansen, P. J. 1991. Quantitative importance and trophic role folded with no visible flagella, and may look like the of heterotrophic dinoflagellate in a coastal pelagic web. damaged tail of an appendicularian to a non- Mar. Ecol. Prog. Ser. 73: 253–61. experienced observer (Fig. 5). Hasle, G. R. and Syvertsen, E. E. 1997. Marine Diatoms. In In conclusion, correct identification of species of Tomas, C. R.w (Ed.) Identifying Marine Phytoplankton. this group of heterotrophic dinoflagellates is a critical Academic Press, San Diego, pp. 5–385. step in the evaluation of its role in pelagic food webs. Léger, G. 1971. Les populations phytoplanctoniques au point 42°47′N, 7°29′E. Bouée laboratoire du C.O.M.E.X.O./ C.N.E.X.O. Généralités et premier séjour (21–27 février ACKNOWLEDGMENTS 1964). Bull. Inst Océanogr. Monaco 69: 1–42. This study was supported by Grant-in-aid for Creative Margalef, R. 1963. Scaphodinium mirabile nov. gen. nov. sp., Basic Research (12NP0201, DOBIS) from the MEXT, un nuevo dinoflagelado aberrante del plancton marino. Japan. F.G. acknowledges the financial support by the Miscelánea Zool. Barcelona 1: 1–2. European Commission (ICB2-CT-2001–80002). Dr K Margalef, R. 1969a. Composición específica del fitoplancton Nakata provided samples from cruises of the SOYO de la costa catalano-levantina (Mediterráneo occidental) program by the Japanese National Research Institute en 1962–67. Inv. Pesq. 33: 345–80. of Fisheries Science. Margalef, R. 1969b. Small scale distribution of phytoplankton in western Mediterranean at the end of July. Pubbl. Staz. Zool. Napoli 37 (Suppl.): 40–61. REFERENCES Margalef, R. 1973. Fitoplancton marino de la región de Abboud-Abi Saab, M. 1989. Les dinoflagellés des eaux afloramiento del NW de África. Res. Exped. Cient. B/O côtières libanaises- Espèces rares ou nouvelles du phyto- Cornide 2: 65–94. plancton marin. Leban. Sci. Bull. 5: 5–16. Margalef, R. 1975. Composición y distribución del fitoplanc- Balkis, N. 2000. Five dinoflagellate species new to Turkish ton marino de la región de afloramiento del NW de África. seas. Oebalia 26: 97–108. Res. Exped. Cient. B/O Cornide 4: 145–70. Cachon, J. and Cachon, M. 1967a. Cymbodinium elegans Sournia, A. 1986. Atlas du Phytoplancton Marin, Vol. I: nov. gen. nov. sp. péridinien Noctilucidae Saville-Kent. Introduction, Cyanophycées, Dictyochophycées, Dinophy- Protistologica 3: 313–8. cées et Raphidophycées. Editions du Centre National de la Cachon, J. and Cachon, M. 1967b. Contribution à l’étude des Recherche Scientifique, Paris, 219 pp. Noctilucidae Saville-Kent, I. Les Kofoidininae Cachon J. et Stoyanova, A. P. 1999. New representatives of noctilucales in M. Évolution, morphologique et systématique. Protistolog- the Bulgarian Black Sea coastal water. Comptes Rend. ica 3: 427–44. Acad. Bulgare Sci. 52: 119–22. Cachon, J. and Cachon, M. 1969. Contribution à l’étude des Taylor, F. J. R. 1976. Dinoflagellates from the International Noctilucidae Saville-Kent. Évolution, morphologique, Indian Ocean Expedition. A report on material collected by cytologie, systématique. II. Les Leptodiscinae Cachon J. et R/V ‘Anton Bruun’ 1963–64. Biblioteca Bot. 132: 1–234. M. Protistologica 5: 11–33. Cachon, J. and Cachon-Enjumet, M. 1964. Leptospathium navicula nov. gen., nov. sp. et Leptophyllus dasypus nov.