Three freshwater Ellerbeckia taxa found in Japan

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1 140 Diatom 30: December 2014 Hiroyuki Tanaka and Tamotsu Nagumo Three freshwater Ellerbeckia taxa found in Japan Hiroyuki Tanaka 1 and Tamotsu Nagumo 2 1 Maebashi Diatom Institute, 57 3 Kawamagari, Maebashi, Gunma , Japan guntana@green.ocn.ne.jp 2 Department of Biology, The Nippon Dental University, Fujimi , Chiyoda-ku, Tokyo , Japan Abstract An investigation of freshwater Ellerbeckia species in Japan was undertaken with three taxa, E. arenaria f. arenaria, E. arenaria f. teres and E. sp., reported herein. Recent E. arenaria f. arenaria was found at one site in Lake Yamanaka, recent E. arenaria f. teres was also found at one site in Lake Akan, fossil E. arenaria f. teres was found in Early Miocene to Pleistocene sediments from 12 localities and E. sp. was found in Early Miocene sediment. All three taxa are illustrated using LM and SEM images, with an additional stereomicroscope photograph for one taxon. Key index words: Ellerbeckia, fossil, freshwater, Japan, recent Introduction Genus Ellerbeckia R.M.Crawford was established by Crawford (1988) using genus type E. arenaria (Moore ex Ralfs) R.M.Crawford and at the same time the transference of Melosira teres Brun to E. arenaria f. teres (Brun) R.M.Crawford was proposed. These are freshwater species. Later, Crawford & Sims (2006) included some marine species into Ellerbeckia. Because E. arenaria f. teres is a diatom found in cold environments that contain tundra pollen (Lortie & Richard 1986, described as Melosira teres from Lake Boucané, Canada), it may be a good taxon to indicate cold water environments. In Japan, freshwater Ellerbeckia species were reported as Melosira arenaria Moore from the Nakayama deposit, Oita by Okuno (1952) with an LM photograph. It is the same deposit as the Nobaru Formation of this report. Recently, Kobayasi et al. (2006) reported Ellerbeckia arenaria f. teres from two localities, Lake Akan and Onogami Formation. Very recently, Tanaka (2014) showed photographs of Ellerbeckia arenaria f. arenaria and E. arenaria f. teres from seven localities with brief morphological descriptions in Japanese, but did not include E. sp. which is included in the present study. In this paper, the authors show the morphology and differences of these three Ellerbeckia taxa using LM, SEM and stereomicroscope photographs. We have found living E. arenaria f. arenaria from only one location, Lake Yamanaka, as previously reported in Tanaka (2014). Ellerbeckia arenaria f. teres, on the other hand, was Received 23 May 2014 Accepted 7 August 2014 found from 13 localities of freshwater materials, one as a living diatom and the others as fossil specimens. Fossil E. arenaria f. teres was found all over Japan in sites ranging from Miocene to Pleistocene, though the specimens exhibited slight morphological differences in the samples from the Onikobe Formation and the Shibusawa lacustrine deposit. In addition, an unidentified taxon similar to E. arenaria f. teres was found from Early Miocene sediment of the Rokkakuzawa Formation. Materials and Method The samples investigated were from two recent localities and 13 fossil localities which are shown in Table 1, 2 and Figure 1, all taken by the first author. In one very unique locality in the Hitoyoshi Formation many Ellerbeckia arenaria f. teres were found gathered together in pebble-size masses, spotted in muddy sediment of narrow horizon (Fig. 32). The samples are to be housed in the Department of Botany, National Museum of Nature and Science in Tsukuba, Ibaraki Prefecture, Japan. Samples were boiled in a 30% H 2 O 2 solution to separate the sediment particles from the diatom valves and then washed several times with distilled water. Some samples were then sifted to separate small and large particles using 63 and 212 mesh. The cleaned material was mounted in Pleurax or Styrax. Stereomicroscope observations were made using a Leica MZ-75 and LM observations using a Nikon Apophot microscope with a plan-apochromat 100 oil immersion objective lens (NA 1.4). SEM observations were made using a Hitachi S-4000 field emission microscope at the Nippon Dental University. Terminology is based on Crawford & Sims (2006).

2 Freshwater Ellerbeckia in Japan 141 Table 1. Ages, localities and references of freshwater Ellerbeckia species in Japan. Taxa Localities Ages Location number of Fig. 1 Figs References E. arenaria f. arenaria Lake Yamanaka Recent Tanaka (2014) Lake Akan Recent 1 Kawashima & Kobayasi (1993), Kobayasi et al. (2006) Onikobe Formation Tanaka (2014) Nobaru Formation , 13, 16 Tanaka et al. (2004), Tanaka (2014) Onogami Formation Pleistocene Tanaka & Kobayasi (1995), Kobayasi et al (2006), Tanaka (2014) Shibusawa lacustrine deposit 7 25 Nagumo & Tanaka (2001) E. arenaria f. teres Hitoyoshi Formation Tanaka & Kitabayashi (2012), Tanaka (2014) Takawashi lacustrine deposit Tanaka et al. (2011) Tsubusagawa Formation Kosaka Member Pliocene 8 38 Tanaka & Kobayasi (1996), Tanaka (2014) Ningyotoge Formation Tanaka et al. (2008), Tanaka (2014) (Takashimizu Member) Miyata Formation Mio-Pliocene 4 17, Tanaka (2014) Futoro Formation Miocene Hachiya Formation E. sp. Rokkakuzawa Formation Miocene Table 2. Localities and samples. Localities and sampling sites Sample numbers Lake Yamanaka Bottom mud of Lake Yamanaka, Yamanashi YAM-101 Lake Akan Bottom mud of Lake Akan, Hokkaido AKN-101 Onikobe Formation Osawa River, Osaki, Miyagi ONI-101 Nobaru Formation Otori, Kitsuki, Oita OTR-101 Onogami Formation Onogami, Shibukawa, Gunma ONO-204 Shibusawa lacustrine deposit Shibusawa, Ueda, Nagano SIB-001 Hitoyoshi Formation Hitoyoshi, Kumamoto KUM-106 Takawashi lacustrine deposit Owashi, Gujo, Gifu SIR-102 Tsubusagawa Formation Amari River, Usa, Oita OIT-207 Kosaka Member Kosakahigashichi, Saku, Nagano KOS-201 Ningyotoge Formation (Takashimizu Member) North of Ningyotoge, Misasa, Tottori NIG-204 Miyata Formation Hinokinaimatazawa, Senboku, Akita MIY-104 Futoro Formation Baikatsu, Setana, Hokkaido SET-307 Rokkakuzawa Formation Fukaura, Aomori ROK-001 Hachiya Formation Daimonnishi, Minokamo, Gifu HAC-002

3 142 Hiroyuki Tanaka and Tamotsu Nagumo Fig. 1. Localities of sampling sites, : recent materials, : fossil materials. 1: Lake Akan; 2: Futoro Formation; 3: Rokkakuzawa Formation; 4: Miyata Formation; 5: Onikobe Formation; 6: Onogami Formation; 7: Shibusawa lacustrine deposit; 8: Kosaka Member; 9: Lake Yamanaka; 10: Takawashi lacustrine deposit; 11: Hachiya Formation; 12: Ningyotoge Formation; 13: Nobaru Formation; 14: Tsubusagawa Formation; 15: Hitoyoshi Formation. Results and Discussion As mentioned above, Ellerbeckia arenaria f. arenaria was found only as a living diatom while E. arenaria f. teres was found as both living and fossil, and E. sp. only as fossil. The morphology of the three taxa are as follows: Ellerbeckia arenaria (Ralfs) R.M.Crawford f. arenaria was found in only one locality, from recent bottom material of Lake Yamanaka, Yamanashi Prefecture. The taxon has large cylindrical valves μm in diameter, μm in height (Figs 2, 4). Valve faces are almost flat with a radial structure, 6 8 in 10 μm at the margin (Fig. 4). Mantles with aroelae rows usually arranged in what appears as diagonal intersecting (Fig. 3). SEM external view shows slightly convex or concave valve faces with cameo/intaglio structures made up of furrows (Fig. 6) and complicated shaped spines located at the valve face/ mantle junction (Fig. 5). Areolae are occluded vela on external surface and with small round openings of porelliportulae in some areolae rows (Fig. 5). Internally, the porelliportulae straddle two ridges (Fig. 7) each having two pinhole pores (Fig. 8). Areolae rows are separated by ridges parallel with pervalver axis, ca. 24 in 10 μm, in rare cases, the internal ridges show an irregular pattern in a small range. Ellerbeckia arenaria f. teres (Brun) R.M.Crawford found from Miocene sediments (2 localities), Pliocene sediments (6 localities: including Mio-Pliocene), Pleistocene sediments (4 localities) and recent bottom material of Lake Akan. The taxon has large cylindrical valves μm in diameter, μm in height (Figs 9, 13 14, 18 19, 22, 24, 26, 28 29, 36). Valve faces have short radial structures on the margin (Figs 9, 18, 28), 6 10 in 10 μm. Mantles are made up of areolae rows usually arranged in a diagonally intersecting pattern (Fig. 10). SEM external view shows slightly convex or concave valve faces with cameo/intaglio structures on circumference (Figs 11, 20 21, 25, 27, 37), areolae occluded vela and small round openings of porelliportulae in some areolae rows (Fig. 16). SEM internal views (Figs 12, 23, 30, 33, 38) of whole valve. Two enlarged internal views of mantle (Figs 34, 39) showing areolae rows on mantle separated by ridges parallel with straight pervalver axis, in 10 μm. The porelliportulae straddle four ridges (Figs 34, 39) and have some pinhole pores near the top (Fig. 34). In rare cases, internal ridges form an irregular pattern in a small range (Fig. 17) on both fossil and recent specimens. The Onikobe Formation, in particular, produced a number of specimens with ridges of the inner mantle swelled (Fig. 31). About half of the specimens from the Shibusawa lacustrine deposit showed a unique feature involving the combination of spiral porelli-portulates together with the usual straight ones (Fig. 35), characteristics in line with E. arenaria f. teres. Ellerbeckia sp. specimens from the Rokkakuzawa Formation under LM look very similar to E. arenaria f. teres with large cylindrical valves μm in diameter, ca. 24 μm in height (Fig. 40) having mantles with aroelae rows usually arranged in a diagonally intersecting pattern. SEM observation shows cameo/intaglio structures present on the margin of the valve faces externally, ca. 9 in 10 μm, areolae rows separated by ridges parallel with pervalver axis internally, 24 in 10 μm. This taxon usually exhibits no porelliportulae (Fig. 41) though they sometimes do exist straddling four or five ridges (Fig. 42). As all Ellerbeckia species have porelliportulae, with E. arenaria f. arenaria straddle two ridges and E. arenaria f. teres straddle four, the authors consider this taxon in need of more investigation.

Freshwater Ellerbeckia in Japan 143 Figs 2 8. Ellerbeckia arenaria f. arenaria from Lake Yamanaka. Fig. 2. Girdle view of chained valves, LM, scale bar b; Fig. 3. Enlarged view of part of Fig.

4 Freshwater Ellerbeckia in Japan 143 Figs 2 8. Ellerbeckia arenaria f. arenaria from Lake Yamanaka. Fig. 2. Girdle view of chained valves, LM, scale bar b; Fig. 3. Enlarged view of part of Fig. 2 showing areolae rows arranged in a diagonally intersecting pattern, LM, scale bar a; Fig. 4. Valve view with radial furrow structure on the valve face, LM, scale bar b; Fig. 5. Part of sibling valves showing linking spines (arrow) and opening of a porelliportula (arrowhead), SEM, scale 2 μm; Fig. 6. External valve face (broken) with cameo/intaglio structures made up of furrows, SEM, scale 10 μm; Fig. 7. Internal view of mantle, porelliportulae (arrowheads), SEM, scale 5 μm; Fig. 8. Detailed view of a porelliportula of Fig. 7, pinhole pores (arrowheads), SEM, scale 0.5 μm. Figs E. arenaria f. teres from Nobaru Formation. Fig. 9. Valve view with radial stracture of furrows in

144 Hiroyuki Tanaka and Tamotsu Nagumo Figs 18 20. Ellerbeckia arenaria f. teres from Hachiya Formation. Fig. 18. Valve view, LM, scale bar a; Fig. 19.

5 144 Hiroyuki Tanaka and Tamotsu Nagumo Figs Ellerbeckia arenaria f. teres from Hachiya Formation. Fig. 18. Valve view, LM, scale bar a; Fig. 19. Girdle view of chained valves, LM, scale bar a; Fig. 20. External oblique view of convex valve, SEM, scale 10 μm. Figs Ellerbeckia arenaria f. teres from Ningyoutoge Formation. Fig. 21. External oblique view of convex valve, SEM, scale 20 μm; Fig. 22. Girdle view, LM, scale bar b. Fig. 23. Ellerbeckia arenaria f. teres from Kosaka Member. Internal oblique view of valve, SEM, scale 20 μm. Figs Ellerbeckia arenaria f. teres from Tsubusagawa Formation. Fig. 24. Girdle view, LM, scale bar b; Fig. 25. External oblique view of concave valve, SEM, scale 20 μm. Figs Ellerbeckia arenaria f. teres from Miyata Formation. Fig. 26. Girdle view, LM, scale bar b; Fig. 27. Broken sibling valves showing cameo/intaglio structure on circumference, SEM, scale 10 μm. the marginal valve face, LM, scale bar b; Fig. 10. Enlarged view of mantle showing areolae rows arranged in a diagonally intersecting pattern, porelliportulae (arrowheads), LM, scale bar a; Fig. 11. Slightly convex external valve face with intaglio structures at the valve margin, SEM, scale 20 μm; Fig. 12. Internal oblique view of valve, SEM, scale 20 μm. Figs E. arenaria f. teres from Onogami Formation. Same valve different focal planes, LM, scale bar b. Figs E. arenaria f. teres from Takawashi lacustrine deposit. Fig. 15. External girdle view, SEM, scale 20 μm; Fig. 16. Enlarged view of part of Fig. 15 showing outer openings of porelliportulae (arrowheads), SEM, scale 2 μm. Fig. 17. E. arenaria f. teres from Miyata Formation. Internal view of a part of mantle showing irregular rows of ridges, SEM, scale 5 μm.

Freshwater Ellerbeckia in Japan 145 Figs 28 31. Ellerbeckia arenaria f. teres from Onikobe Formation. Fig. 28. Valve view with radial structure of furrows in the marginal valve face, LM; Fig. 29.

6 Freshwater Ellerbeckia in Japan 145 Figs Ellerbeckia arenaria f. teres from Onikobe Formation. Fig. 28. Valve view with radial structure of furrows in the marginal valve face, LM; Fig. 29. Girdle view of chained valves, LM; Fig. 30. Internal oblique view of valve, SEM, scale 10 μm; Fig. 31. Enlarged view of part of Fig. 30 showing irregular and swelled ridges, SEM, scale 2 μm. Figs Ellerbeckia arenaria f. teres from Hitoyoshi Formation, Fig. 32. Assemblage view of raw material before handling, Ellaerbeckia species (arrows), Stereomicroscope, scale 300 μm; Fig. 33. Internal oblique view of a shallow valve, SEM, scale 20 μm; Fig. 34. Detailed view of a porelliportula, pinhole pores (arrowheads), and internal areolae rows separated by ridges, SEM, scale 1 μm. Fig. 35. Ellerbeckia arenaria f. teres from Shibusawa lacustrine deposit. Part of inner mantle showing porelliportulae with spiral ridges (arrowhead a) and straight ridges (arrowhead b), SEM, scale 5 μm. Figs Ellerbeckia arenaria f. teres from Futoro Formation. Fig. 36. Girdle view of chained valves, LM; Fig. 37. External oblique view of convex valve face, SEM, scale 20 μm; Fig. 38. Internal oblique view of a deep valve, SEM, scale 10 μm; Fig. 39. Detailed view of a porelliportula of Fig. 38 (broken tip) straddling four ridges, SEM, scale 1 μm. Figs Ellerbeckia sp. from Rokkakuzawa Formation. Fig. 40. Girdle view of valves, LM; Fig. 41. Part of inner mantle without porelliportulae, SEM, scale 5 μm; Fig. 42. Two porelliportulae (broken tips), SEM, scale 2 μm.

7 146 Hiroyuki Tanaka and Tamotsu Nagumo References Crawford, R.M A reconsideration of Melosira arenaria and M. teres; resulting in a proposed new genus Ellerbeckia. In: Round, F.E. (ed.) Algae and the aquatic environment. pp Biopress, Bristol. Crawford, R.M. & Sims, P.A The diatoms Radialiplicate sol (Ehrenberg) Glezer and R. clavigera (Grunow) Glezer and their transfer to Ellerbeckia, Crawford, thus a genus with freshwater and marine representatives. Nova Hedwigia, Beiheft 130: Kawashima, A. & Kobayasi, H Diatoms from Akan-ko (Lake Akan) in Hokkaido, Japan. 1. Centric diatoms. Natural Environmental Science Research 6: (in Japanese with English abstract) Kobayasi, H., Idei, M., Mayama, S., Nagumo, T. & Osada, K H.Kobayasi s atlas of Japanese diatoms based on electron microscopy pp. Uchida Rokakuho, Tokyo. (in Japanese and English explanation of plates) Lortie, G. & Richard, P.J.H Late-glacial diatom and pollen stratigraphy from Lake Boucané, Southeastern Québec, Canada. In: Ricard, M. (ed.) Proceedings of the 8th International Diatom Symposium, Paris. Koeltz Scientific Books, Koenigstein. Nagumo, T. & Tanaka, H Diatoms from the Pleistocene lacustrine deposit in eastern Sanada Town, Nagano Prefecture, Japan. Bulletin of the Nippon Dental University General Education 30: (in Japanese with English summary) Okuno, H Atlas of fossil diatoms from Japanese diatomite deposits. 51 pp. 29 pls. Botanical Institute, Faculty of Textile Fibers, Kyoto University of Industrial Arts and Textile Fibers, Kyoto. Tanaka, H Atlas of freshwater fossil diatoms in Japan Including related recent taxa. 602 pp. Uchida Rokakuho Publishing, Tokyo. (in Japanese and English explanation of plates) Tanaka, H. & Kobayasi, H Diatoms from the Onogami Formation, an Early Pleistocene lacustrine deposit, central Japan. Diatom 10: (in Japanese with English abstract) Tanaka, H. & Kobayasi, H Diatoms from the Kohsaka Conglomerate Member (the early Pliocene series). central Japan. Chigaku Kenkyu 45: (in Japanese with English abstract) Tanaka, H., Nagumo, T., Kashima, K. & Mitsuhashi, F Pliocene diatoms from freshwater diatomite in Yamaga Town, Kyushu, Japan. Diatom 20: Tanaka, H., Suzuki, H. & Nagumo, T Fossil freshwater diatoms from the Ningyotoge Formation (Late Miocene-Pliocene) at the Okayama and Tottori Prefecture boundary, Japan. Diatom 24: (in Japanese with English abstract) Tanaka, H., Watanabe, T. & Nagumo, T Fossil diatoms from lacustrine deposit in Owashi, northern Gujo City, Gifu Prefecture, Japan. Bulletin of the Mizunami Fossil Museum 37: (in Japanese with English abstract) Tanaka, H. & Kitabayashi, E Freshwater fossil diatoms, Ellerbeckia, from the Hitoyoshi Formation (Upper Pliocene) in Kumamoto Prefecture, Japan. Chigaku Kenkyu 60: (in Japanese with English abstract)

Stephanodiscus uemurae, a new Mio-Pliocene diatom species from the Miyata Formation, Akita Prefecture, northern Honshu, Japan

Diatom 25 :4551. December 2009 Stephanodiscus uemurae, a new Mio-Pliocene diatom species from the Miyata Formation, Akita Prefecture, northern Honshu, Japan Hiroyuki Tanaka 1 and Tamotsu Nagumo 2 1 Maebashi