Advertisement

Journal of Oceanography

, Volume 66, Issue 6, pp 755–771 | Cite as

Species diversity of the genus Skeletonema (Bacillariophyceae) in the industrial harbor Dokai Bay, Japan

  • Machiko YamadaEmail author
  • Eri Katsuki
  • Mayuko Otsubo
  • Mayumi Kawaguchi
  • Kazuhiko Ichimi
  • Hideki Kaeriyama
  • Kuninao Tada
  • Paul J. Harrison
Article

Abstract

Seven Skeletonema species were identified at one station in the industrial harbor Dokai Bay, Japan, in October 2007 and then monthly from January 2008 to December 2009 by morphological scanning electron microscopy observations and molecular analyses of mainly the large subunit (LSU) rDNA. We refer to one species identified as S. dohrnii using LSU rDNA, but as S. marinoi using the small subunit (SSU) rDNA and consequently we use the term S. marinoi-dohrnii complex. This is the first time that S. ardens, S. costatum s.s., and S. pseudocostatum have been recorded in Japan and that S. menzelii and S. tropicum have been identified by molecular methods in Japan. The S. marinoi-dohrnii complex was isolated with high frequency all year-round, and S. japonicum was also isolated with high frequency but not so in summer. S. Tropicum was isolated from September to December, but S. ardens and S. costatum s.s. were isolated only when the water temperature exceeded 20°C. S. pseudocostatum bloomed just once, in summer, but S. menzelii was isolated in May and again in October. The continuous year-round occurrence of S. costatum s.l. in the bay is supported by the succession of these seven species. Six of the species, except S. menzelii, were important components of algal blooms in the bay. One to four species of Skeletonema were isolated every month. Monthly species diversity was higher when S. ardens, S. costatum s.s., and S. tropicum that are usually associated with tropical or subtropical waters, were isolated. In general, species diversity of the genus Skeletonema was very high in Dokai Bay.

Keywords

Skeletonema species diversity isolation characteristics Dokai Bay LSU rDNA SSU rDNA SEM 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bergesch, M., M. Garcia and C. Odebrecht (2009): Diversity and morphology of Skeletonema species in southern Brazil, southwestern Atlantic ocean. J. Phycol., 45, 1348–1352.CrossRefGoogle Scholar
  2. Chen, G. F., G. C. Wang., B. Y. Zhang and X. L. Fan (2007): Morphological and phylogenetic analysis of Skeletonema costatum-like diatoms (Bacillariophyta) from the China Sea. Eur. J. Phycol., 42, 163–175.CrossRefGoogle Scholar
  3. Cheng, J., L. Yang, L. Junrong, G. Yahui, W. Peng, K.-C. Ho and L. Xin (2008): Morphological variability and genetic diversity in five species of Skeletonema (Bacillariophyta). Prog. Nat. Sci., 18, 1345–1355.CrossRefGoogle Scholar
  4. Cleve, P. T. (1900): Notes on some Atlantic plankton-organisms. Kongl. Svenska Vetensk. Akad. Handl., 34, 3–31.Google Scholar
  5. Ellegaard, M., A. Godhe, K. Härnström and M. McQuoid (2008): The species concept in a marine diatom: LSU rDNAbased phylogenetic differentiation in Skeletonema marinoi/dohrnii (Bacillariophyceae) is not reflected in morphology. Phycologia, 47, 156–167.CrossRefGoogle Scholar
  6. Gallagher, J. C. (1980): Population genetics of Skeletonema costatum (Bacillariophyceae) in Narragansett Bay. J. Phycol., 16, 464–474.CrossRefGoogle Scholar
  7. Gallagher, J. C. (1982): Physiological variation and electrophoretic banding patterns of genetically different seasonal populations of Skeletonema costatum (Bacillariophyceae). J. Phycol., 18, 148–162.CrossRefGoogle Scholar
  8. Gallagher, J. C. (1994): Genetic structure of microalgal populations. I. Problems associated with the use of strains as terminal taxa. p. 69–86. In Proceedings of the 11th International Diatom Symposium 1990, ed. by J. P. Kociolek, California Academy of Sciences, San Francisco, CA, U.S.A.Google Scholar
  9. Garrison, D. L. (1984): Chapter 1, Planktonic diatoms. p. 1–17. In Marine Plankton Life Cycle Strategies, ed. by K. A. Steidinger and L. M. Walker, CRC Press, Florida, U.S.A.Google Scholar
  10. Godhe, A., M. R. McQuoid, I. Karunasagar, I. Karunasagar and A.-S. Rehnstam-Holm (2006): Comparison of three common molecular tools for distinguishing among geographically separated clones of the diatom Skeletonema marinoi Sarno et Zingone (Bacillariophyceae). J. Phycol., 42, 280–291.CrossRefGoogle Scholar
  11. Greville, R. K. (1866): Description of new and rare diatoms. Series 20. Trans. Micr. Soc. London, n.s., 14, 77–86.Google Scholar
  12. Guillard, R. R. L., E. J. Carpenter and B. E. F. Reimann (1974): Skeletonema menzelii sp. nov., a new diatom from the western Atlantic Ocean. Phycologia, 13, 131–138.CrossRefGoogle Scholar
  13. Hargraves, P. E. and F. W. French (1983): Diatom resting spore: significance and strategies. p. 49–68. In Survival Strategies of the Algae, ed. by G. A. Fryxell, Cambridge University Press, New York, U.S.A.Google Scholar
  14. Hasle, G. R. (1973): Morphology and taxonomy of Skeletonema costatum (Bacillariophyceae). Norw. J. Bot., 20, 109–137.Google Scholar
  15. Hulburt, E. M. and R. R. L. Guillard (1968): The relationship of the distribution of the diatom Skeletonema tropicum to temperature. Ecology, 49, 337–339.CrossRefGoogle Scholar
  16. Imai, I., K. Ito and M. Anraku (1984): Extinction dilution method for enumeration of dormant cells of red tide organisms in marine sediments. Bull. Plankton Soc. Japan, 31, 123–124.Google Scholar
  17. Kimura, M. (1980): A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol., 16, 111–120.CrossRefGoogle Scholar
  18. Kooistra, W. H. C. F., D. Sarno, S. Balzano, H. Gu, R. A. Andersen and A. Zingone (2008): Global diversity and biogeography of Skeletonema species (Bacillariophyta). Protist, 159, 177–193.CrossRefGoogle Scholar
  19. Medlin, L., H. J. Elwood, S. Stickel and M. L. Sogin (1988): The characterization of enzymatically amplified eukaryotic 16-like rRNA-coding regions. Gene, 71, 491–499.CrossRefGoogle Scholar
  20. Medlin, L. K., H. J. Elwood, S. Stickel and M. L. Sogin (1991): Morphological and genetic variation within the diatom Skeletonema costatum (Bacillariophyta): evidence for a new species, Skeletonema pseudocostatum. J. Phycol., 27, 514–524.CrossRefGoogle Scholar
  21. Nagumo, T. (1995): Simple and safe cleaning methods for diatom sample. Diatom, 10, 88.Google Scholar
  22. Okaichi, T., S. Nishio and Y. Imatomi (1983): Mass culture of marine phytoflagellates: an approach to new sources of biologically active compounds. p. 141–144. In IUPAC Pesticide Chemistry, Vol. 2, ed. by J. Miyamoto and P. C. Kearney, Pergamon Press, New York, U.S.A.Google Scholar
  23. Orsini, L., D. Sarno, D. Procaccini, R. Poletti, J. Dahlmann and M. Montresor (2002): Toxic Pseudo-nitzschia multistriata (Bacillariophyceae) from the Gulf of Naples: morphology, toxin analysis and phylogenetic relationships with other Pseudo-nitzschia species. Eur. J. Phycol., 37, 247–257.CrossRefGoogle Scholar
  24. Ribera, d’A. M., F. Conversano, F. Corato, P. Licandro, O. Mangon, D. Marino, M. G. Mazzocchi, M. Modigh, M. Montresor, M. Nardella, V. Saggiomo, D. Sarno and A. Zingone (2004): Seasonal patterns in plankton communities in a pluriannual time series at a coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends. Sci. Mar., 68(Suppl. 1), 65–83.Google Scholar
  25. Saggiomo, M., W. H. C. F. Kooistra, D. Sarno, M. Montresor, C. L. Burn, J. Cloern, P. Hargraeves and A. Zingone (2006): Differences in Skeletonema distribution among three distant temperate coastal sites. J. Phycol., 42, 31–32.Google Scholar
  26. Saitou, N. and M. Nei (1987): The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol., 4, 406–425.Google Scholar
  27. Sarno, D., W. H. C. F. Kooistra, L. K. Medlin, I. Percopo and A. Zingone (2005): Diversity in the genus Skeletonema (Bacillariophyceae). II. An assessment of the taxonomy of S. costatum-like species with the description of four new species. J. Phycol., 41, 151–176.CrossRefGoogle Scholar
  28. Sarno, D., W. H. C. F. Kooistra, P. E. Hargraves and A. Zingone (2007): Diversity in the genus Skeletonema (Bacillariophyceae). III. Phylogenetic position and morphology of Skeletonema costatum and Skeletonema grevillei, with the description of Skeletonema ardens sp. Nov. J. Phycol., 43, 156–170.CrossRefGoogle Scholar
  29. Suksomjit, M., K. Ichimi, K. Hamada, M. Yamada, K. Tada and P. J. Harrison (2009): Ammonium accelerates the growth rate of Skeletonema spp. in the phytoplankton assemblage in a heavily eutrophic embayment, Dokai Bay, Japan. La mer, 47, 89–101.Google Scholar
  30. Takano, H. (1981): New and rare diatoms from Japanese marine waters—VII. Ten species from neritic waters. Bull. Tokai Reg. Fish. Res. Lab., 105, 45–57.Google Scholar
  31. Tamura, K., J. Dudley, M. Nei and S. Kumar (2007): MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol. Biol. Evol., 24, 1596–1599.CrossRefGoogle Scholar
  32. Thompson, J. D., D. G. Higgins and T. J. Gibson (1994): CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673–4680.CrossRefGoogle Scholar
  33. Ueno, S. (1993): On the occurrence of a tropical marine diatom Skeletonema tropicum in coastal waters of Japan, with some morphological remarks. Bull. Plankton Soc. Japan, 39, 97–106.Google Scholar
  34. Yamada, M. (1987): A study for a classification method of the eutrophication with phytoplankton. Doctoral thesis, Kyoto University, 94 pp. (in Japanese).Google Scholar
  35. Yamada, M. (2000): Chapter 12. Dokai Bay. p. 161–173. In Water Pollution Control Policy and Management: The Japanese Experience, ed. by M. Okada and S. A. Peterson, Gyosei, Tokyo.Google Scholar
  36. Yamada, M. and Y. Kaziwara (2004): Characteristics of phytoplankton occurrence in the hyper-eutrophic environment, Dokai Bay, Japan. Umi no Kenkyu, 13, 281–293 (in Japanese with English abstract).Google Scholar
  37. Yamada, M., M. Katsuki, M. Otsubo, K. Hamada, N. Ueda and S. Montani (2009): Survival strategy of tropical and subtropical marine diatom Skeletonema tropicum in temperate coastal small bay (Dokai Bay), Japan. Umi no Kenkyu, 18, 157–167 (in Japanese with English abstract).Google Scholar
  38. Zingone, A., I. Percopo, P. A. Sims and D. Sarno (2005): Diversity in the genus Skeletonema (Bacillariophyceae). I. A reexamination of the type material of S. costatum with the description of S. grevillei sp. nov. J. Phycol., 41, 140–150.CrossRefGoogle Scholar

Copyright information

© The Oceanographic Society of Japan and Springer 2010

Authors and Affiliations

  • Machiko Yamada
    • 1
    Email author
  • Eri Katsuki
    • 1
  • Mayuko Otsubo
    • 1
  • Mayumi Kawaguchi
    • 1
  • Kazuhiko Ichimi
    • 2
  • Hideki Kaeriyama
    • 3
  • Kuninao Tada
    • 4
  • Paul J. Harrison
    • 5
  1. 1.Faculty of Human Environmental ScienceFukuoka Women’s UniversityKasumigaoka, Higashi-ku, FukuokaJapan
  2. 2.Aji Marine Station, Seto Inland Sea Regional Research CenterKagawa UniversityAji, Takamatsu, KagawaJapan
  3. 3.Coastal Fisheries and Aquaculture DivisionSeikai National Fisheries Research InstituteTaira, Nagasaki, NagasakiJapan
  4. 4.Faculty of AgricultureKagawa UniversityMiki-cho, Kita-gun, KagawaJapan
  5. 5.Division of EnvironmentHong Kong University of Science and TechnologyKowloon, Hong KongChina

Personalised recommendations