Morphologic and genetic variability in the marine planktonic ciliate Laboea strobila Lohmann, 1908 (Ciliophora, Oligotrichia), with notes on its ontogenesis

Journal of Eukaryotic Microbiology

Volumn 51, Issue 3, 2004, Pages 267-281

  Agatha, Sabine ^a   Strüder Kypke, Michaela C ^b   Beran, Alfred ^c  

^a UNIVERSITY OF SALZBURG   (Austria)

^b UNIVERSITY OF GUELPH   (Canada)

^c Laboratorio di Biologia Marina   (Italy)

Author keywords

Intraspecific variability; Live observation; Phylogeny; Protargol impregnation; Scanning electron microscopy; SSrRNA; Strombidiidae; Taxonomy

Indexed keywords

RIBOSOME RNA; SEA WATER;

CILIATE; ECOMORPHOLOGY; GENETIC VARIATION; ONTOGENY; PHYLOGENETICS; TAXONOMY;

ANIMAL; ARTICLE; CHEMISTRY; CILIATE; CLASSIFICATION; CYTOLOGY; GENETIC VARIABILITY; GENETICS; PLANKTON;

ANIMALS; CILIOPHORA; PLANKTON; RNA, RIBOSOMAL; SEAWATER; VARIATION (GENETICS);

ATLANTIC OCEAN; IRISH SEA; MEDITERRANEAN SEA; NORTH SEA;

CILIOPHORA; LABOEA; LABOEA STROBILA; OLIGOTRICHIA; OLIGOTRICHS; PROTOZOA; STROMBIDIIDAE; STROMBIDIUM;

EID: 2542431290     PISSN: 10665234     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2004.tb00567.x     Document Type: Article

References (89)

1. Aescht, E. 2001. Catalogue of the generic names of ciliates (Protozoa, Ciliophora). Denisia, 1:1-350.
2. Agatha, S. 2001. Oligotrichea (aloricate species). In: Costello, M. J., Emblow, C. S. & White, R. (ed.), European Register of Marine Species. A Check-list of the Marine Species in Europe and a Bibliography of Guides to Their Identification. Patrimoines naturels, 50:42-44.
3. Agatha, S. 2003. Morphology and ontogenesis of Novistrombidium apsheronicum nov. comb. and Strombidium arenicola (Protozoa, Ciliophora): a comparative light microscopical and SEM study. Europ. J. Protistol., 39:245-266.
4. Alekperov, I. Kh. & Asadullayeva, E. S. 1997. New and little-known ciliates (orders Nassulida-Oligotrichida) from the Caspian Sea Apsheronian coast. Communication 2. Zool. Zh., 76:1411-1417. (in Russian with English summary)
5. Alekperov, I. H. & Mamajeva, N. V. 1992. Planktonic infusoria from the Chuckchee and the Bering Seas. Zool. Zh., 71:5-14. (in Russian with English summary)
6. Anigstein, L. 1913. Über Strombidium testaceum nov. spec. eine marine oligotriche Ciliate. Arch. Protistenk., 32:79-110 + Plate 1, 2.
7. Bernard, C. & Rassoulzadegan, F. 1994. Seasonal variations of mixotrophic ciliates in the northwest Mediterranean Sea. Mar. Ecol. Prog. Ser., 108:295-301.
8. Bernhard, D., Stechmann, A., Foissner, W., Ammermann, D., Hehn, M. & Schlegel, M. 2001. Phylogenetic relationships within the class Spirotrichea (Ciliophora) inferred from small subunit rRNA gene sequences. Mol. Phylogenet. Evol., 21:86-92.
9. Busch, W. 1921. Studien über Ciliaten des Nordatlantischen Ozeans und Schwarzen Meeres. I. Arch. Protistenk., 42:364-379 + Plate 16, 17.
10. Busch, W. 1930. Ueber marine Strombidium-Arten aus der antarktischen allgemeinen Ostströmung. Abh. Mus. Nat. Heimatk. Magdeburg, 6:83-87.
11. Chang, F. H. 1990. Quantitative distribution of microzooplankton off Westland, New Zealand. New Zealand J. Mar. Freshw. Res., 24:187-195.
12. Claparède, E. & Lachmann, J. 1859. Études sur les infusoires et les rhizopodes. Mém. Inst. natn. Génev., 6 (year 1858):261-482 + Plate 14-24.
13. Corliss, J. O. 1979. The Ciliated Protozoa. Characterization, Classification and Guide to the Literature, 2nd ed. Pergamon Press, Oxford. p. i-xvi + 1-455.
14. De Rijk, P. & De Wachter, R. 1993. DCSE, an interactive tool for sequence alignment and secondary structure research. CABIOS, 9:735-740.
15. Dolan, J. R. & Marrasé, C. 1996. Planktonic ciliate distribution relative to a deep chlorophyll maximum: Catalan Sea, N.W. Mediterranean, June 1993. Deep-Sea Res. I, 42 (year 1995):1965-1987.
16. Elwood, H. J., Olsen, G. J. & Sogin, M. L. 1985. The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Mol. Biol. Evol., 2:399-410.
17. Fauré-Fremiet, E. 1924. Contribution a la connaissance des infusoires planktoniques. Bull. biol. Fr. Belg. Suppl., 6:1-171.
18. Fauré-Fremiet, E. 1970. Remarques sur la systématique des ciliés Oligotrichida. Protistologica, 5 (year 1969):345-352.
19. Fauré-Fremiet, E. & Ganier, M.-Cl. 1970. Structure fine du Strombidium sulcatum Cl. et L. (Ciliata Oligotrichida). Protistologica, 6:207-223.
20. Foissner, W. 1991. Basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa. Europ. J. Protistol., 27:313-330.
21. Foissner, W., Agatha, S. & Berger, H. 2002. Soil ciliates (Protozoa, Ciliophora) from Namibia (Southwest Africa), with emphasis on two contrasting environments, the Etosha region and the Namib Desert. Part I: Text and line drawings. Part II: Photographs. Denisia, 5:1-1459.
22. Fonda Umani, S. & Monti, M. 1991. Microzooplankton populations in the Strait of Magellan. Boll. Oceanol. Teo. Appl., 9:151-162.
23. Guillard, R. R. L. 1995. Culture Methods. In: Hallegraeff, G. M., Anderson, D. M. & Cembella, A. D. (ed.), Manual on Harmful Marine Microalgae. IOC Manuals and Guides, 33:45-62.
24. Hamburger, C. & Buddenbrock, W. v. 1929. Nordische Ciliata mit Ausschluß der Tintinnoidea. Nordisches Plankton. Lipsius and Tischler, Kiel. Zool. Teil, 7:1-152.
25. Hasle, G. R. 1960. Phytoplankton and ciliate species from the tropical Pacific. Skr. Norske Vid.-Akad. Oslo I, 2:5-50.
26. Hofker, J. 1931. Studien über Tintinnoidea. Arch. Protistenk., 75:315-402.
27. Huelsenbeck, J. P. & Ronquist, F. R. 2004. MRBAYES: Bayesian inference of phylogeny. Biometrics, (in press).
28. Ibanez, F. & Rassoulzadegan, F. 1977. A study of the relationships between pelagic ciliates (Oligotrichina) and planktonic nanoflagellates of the neritic ecosystem of the Bay of Villefranche-sur-Mer. Analysis of chronological series. Ann. Inst. océanogr., Paris, 53:17-30.
29. ICZN [= International Commission on Zoological Nomenclature]. 1999. International Code of Zoological Nomenclature. Fourth Edition Adopted by the International Union of Biological Sciences. International Trust for Zoological Nomenclature 1999, London. Tipografia La Garangola, Padova. p. 1-306.
30. James, M. R. & Hall, J. A. 1995. Planktonic ciliated protozoa: their distribution and relationship to environmental variables in a marine coastal ecosystem. J. Plankton Res., 17:659-683.
31. Jerome, C. A. & Lynn, D. H. 1996. Identifying and distinguishing sibling species in the Tetrahymena pyriformis complex (Ciliophora, Oligohymenophorea) using PCR/RFLP analysis of nuclear ribosomal data. J. Eukaryot. Microbiol., 43:492-497.
32. Jonsson, P. R. 1987. Photosynthetic assimilation of inorganic carbon in marine oligotrich ciliates (Ciliophora, Oligotrichina). Mar. Microb. Food Webs, 2:55-67.
33. Kahl, A. 1932. Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 3. Spirotricha. Tierwelt Dtl., 25:399-650.
34. 3):29-146.
35. Krainer, K.-H. 1991. Contributions to the morphology, infraciliature and ecology of the planktonic ciliates Strombidium pelagicum n. sp., Pelagostrombidium mirabile (Penard, 1916) n. g., n. comb., and Pelagostrombidium fallax (Zacharias, 1896) n. g., n. comb. (Ciliophora, Oligotrichida). Europ. J. Protistol., 27:60-70.
36. Krainer, K.-H. 1995. Taxonomische Untersuchungen an neuen und wenig bekannten planktischen Ciliaten (Protozoa: Ciliophora) aus Baggerseen in Österreich. Lauterbornia, 21:39-68.
37. Laval-Peuto, M. & Rassoulzadegan, F. 1988. Autofluorescence of marine planktonic Oligotrichina and other ciliates. Hydrobiologia, 159:99-110.
38. Laval-Peuto, M., Grain, J. & Deroux, G. 1994. Classe des Oligotrichea Bütschli, 1887. Ordres des Oligotrichida Bütschli, 1887 et des Choreotrichida Small et Lynn, 1985. Traité de Zoologie, 2 (2):153-179.
39. Leegaard, C. 1915. Untersuchungen über einige Planktonciliaten des Meeres. Nytt Mag. Naturvid., 53:1-37.
40. Lei, Y., Xu, K. & Song, W. 1999. Free-living ciliates from marine farming ponds. In: Song, W. (ed.), Progress in Protozoology. Qingdao Ocean Univ. Press, Qingdao. p. 269-295. (in Chinese)
41. Levinsen, H., Nielsen, T. G. & Hansen, B. W. 2000. Annual succession of marine pelagic protozoans in Disko Bay, West Greenland, with emphasis on winter dynamics. Mar. Ecol. Prog. Ser., 206:119-134.
42. Lohmann, H. 1908. Untersuchungen zur Feststellung des vollständigen Gehaltes des Meeres an Plankton. Wiss. Meeresunters., Abt. Kiel, 10:129-370.
43. Lynn, D. H. & Gilron, G. L. 1993. Strombidiid ciliates from coastal waters near Kingston Harbour, Jamaica (Ciliophora, Oligotrichia, Strombidiidae). J. mar. biol. Ass. U.K., 73:47-65.
44. Lynn, D. H. & Small, E. B. 2002. Phylum Ciliophora Doflein, 1901. In: Lee, J. J., Leedale, G. F. & Bradbury, P. (ed.), An Illustrated Guide to the Protozoa, 2nd ed. (year 2000) Organisms Traditionally Referred to as Protozoa, or Newly Discovered Groups. Allen Press, Lawrence, Kansas. p. 371-656.
45. Lynn, D. H., Montagnes, D. J. S. & Small, E. B. 1988. Taxonomic descriptions of some conspicuous species in the family Strombidiidae (Ciliophora: Oligotrichida) from the Isles of Shoals, Gulf of Maine. J. mar. biol. Ass. U.K., 68:259-276.
46. Maeda, M. & Carey, P. G. 1985. An illustrated guide to the species of the family Strombidiidae (Oligotrichida, Ciliophora), free-swimming protozoa common in the aquatic environment. Bull. Ocean Res. Inst., Univ. Tokyo, 19:1-68.
47. Mamaeva, N. V. 1989. Ciliated protozoa of the Antarctic region of the Atlantic. Dokl. Akad. Nauk SSSR, 308:503-504.
48. Margalef, R. 1973. Distribución de los ciliados planctónicos en la region de afloramiento del noroeste de África (Campaña "Sahara II" del "Cornide de Saavedra"). Res. Exp. Cient. B/O Cornide, 2:109-124.
49. Martin, A. J. & Montagnes, D. J. S. 1993. Winter ciliates in a British Columbian fjord: six new species and an analysis of ciliate putative prey. J. Eukaryot. Microbiol., 40:535-549.
50. McManus, G. B. & Fuhrman, J. A. 1986. Photosynthetic pigments in the ciliate Laboea strobila from Long Island Sound, USA. J. Plankton Res., 8:317-327.
51. Meunier, A. 1910. Campagne arctique de 1907. Microplankton des mers de Barents et de Kara. Bulens, Bruxelles. p. i-xviii + 1-355.
52. Milani, L., Cabrini, M., Fonda Umani, S. & Honsell, G. 1991. The microzooplankton in a station in the Gulf of Trieste from March 1986 to September 1988: data report. Nova Thalassia, 9 (1987-1988):53-95.
53. Modeo, L., Petroni, G., Bonaldi, M. & Rosati, G. 2001. Trichites of Strombidium (Ciliophora, Oligotrichida) are extrusomes. J. Eukaryot. Microbiol., 48:95-101.
54. Modeo, L., Petroni, G., Rosati, G. & Montagnes, D. J. S. 2003. A multidisciplinary approach to describe protists: redescriptions of Novistrombidium testaceum Anigstein 1914 and Strombidium inclinatum Montagnes, Taylor and Lynn 1990 (Ciliophora, Oligotrichia). J. Eukaryot. Microbiol., 50:175-189.
55. Modigh, M. 2001. Seasonal variations of photosynthetic ciliates at a Mediterranean coastal site. Aquat. Microb. Ecol., 23:163-175.
56. Møller, E. F. & Nielsen, T. G. 2000. Plankton community structure and carbon cycling off the western coast of Greenland, with emphasis on sources of DOM for the bacterial community. Aquat. Microb. Ecol., 22:13-25.
57. Montagnes, D. J. S. & Humphrey, E. 1998. A description of occurrence and morphology of a new species of red water-forming Strombidium (Spirotrichea, Oligotrichia). J. Eukaryot. Microbiol., 45:502-506.
58. Montagnes, D. J. S. & Taylor, F. J. R. 1994. The salient features of five marine ciliates in the class Spirotrichea (Oligotrichia), with notes on their culturing and behaviour. J. Eukaryot. Microbiol., 41:569-586.
59. Montagnes, D. J. S., Lynn, D. H., Stoecker, D. K. & Small, E. B. 1988. Taxonomic descriptions of one new species and redescription of four species in the family Strombidiidae (Ciliophora, Oligotrichida). J. Protozool., 35:189-197.
60. Ota, T. & Taniguchi, A. 2003. Standing crop of planktonic ciliates in the East China Sea and their potential grazing impact and contribution to nutrient regeneration. Deep-Sea Res. II, 50:423-442.
61. Petz, W. 1994. Morphology and morphogenesis of Strombidium kryalis nov. spec. (Ciliophora, Strombidiida) from Antarctic sea ice. Arch. Protistenk., 144:185-195.
62. Petz, W. 1999. Ciliophora. In: Boltovskoy, D. (ed.), South Atlantic Zooplankton I. Backhuys Publ., Leiden. p. 265-319.
63. Petz, W., Song, W. & Wilbert, N. 1995. Taxonomy and ecology of the ciliate fauna (Protozoa, Ciliophora) in the endopagial and pelagial of the Weddell Sea, Antarctica. Stapfia, 40:1-223.
64. Putt, M. 1990a. Abundance, chlorophyll content and photosynthetic rates of ciliates in the Nordic Seas during summer. Deep-Sea Res. Part A, 37:1713-1731.
65. Putt, M. 1990b. Metabolism of photosynthate in the chloroplast-retaining ciliate Laboea strobila. Mar. Ecol. Prog. Ser., 60:271-282.
66. Rassoulzadegan, F. 1977. Évolution annuelle des ciliés pélagiques en Méditerranée nord-occidentale. Ciliés oligotriches "non tintinnides" (Oligotrichina). Ann. Inst. océanogr., Paris, 53:125-134.
67. Sanders, R. W. 1995. Seasonal distributions of the photosynthesizing ciliates Laboea strobila and Myrionecta rubra (= Mesodinium rubrum) in an estuary of the Gulf of Maine. Aquat. Microb. Ecol., 9:237-242.
68. Schlegel, M., Elwood, H. J. & Sogin, M. L. 1991. Molecular evolution in hypotrichous ciliates: sequence of the small subunit ribosomal RNA genes from Onychodromus quadricornutus and Oxytricha granulifera (Oxytrichidae, Hypotrichida, Ciliophora). J. Mol. Evol., 32:64-69.
69. Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics, 18:502-504.
70. Shin, M. K., Hwang, U. W., Kim, W., Wright, A.-D. G., Krawczyk, C. & Lynn, D. H. 2000. Phylogenetic position of the ciliates Phacodinium (order Phacodiniida) and Protocruzia (subclass Protocruziidia) and systematics of the spirotrich ciliates examined by small subunit ribosomal RNA gene sequences. Europ. J. Protistol., 36:293-302.
71. Sime-Ngando, T., Gosselin, M., Juniper, S. K. & Lavasseur, M. 1997. Changes in sea-ice phagotrophic microprotists (20-200 μm) during the spring algal bloom, Canadian Arctic Archipelago. J. Mar. Syst., 11:163-172.
72. Small, E. B. & Lynn, D. H. 1985. Phylum Ciliophora Doflein, 1901. In: Lee, J. J., Hutner, S. H. & Bovee, E. C. (ed.), An Illustrated Guide to the Protozoa. Allen Press, Lawrence, Kansas. p. 393-575.
73. Snoeyenbos-West, O. L. O., Salcedo, T., McManus, G. B. & Katz, L. A. 2002. Insights into the diversity of choreotrich and oligotrich ciliates (Class: Spirotrichea) based on genealogical analyses of multiple loci. Int. J. Syst. Evol. Microbiol., 52:1901-1913.
74. Song, W. 1999. Infraciliature of oligotrichous ciliates at generic level. In: Song, W. (ed.), Progress in Protozoology. Qingdao Ocean Univ. Press, Qingdao. p. 155-176.
75. Song, W. & Wang, M. 1996. Morphogenesis of Strombidium sulcatum during asexual binary division. Prog. Nat. Sci., 6:741-746.
76. Song, W. & Wilbert, N. 1995. Benthische Ciliaten des Süßwassers. In: Röttger, R. (ed.), Praktikum der Protozoologie. Gustav Fischer Verlag, Stuttgart. p. 156-168.
77. Song, W., Zhu, M. & Chen, Z. 1999. Updating the systematics of the planktonic oligotrichous ciliates (Ciliophora, Protozoa) with description of ciliature patterns at generic level. Yellow Sea, 5:77-85.
78. Stoecker, D. K. & Michaels, A. E. 1991. Respiration, photosynthesis and carbon metabolism in planktonic ciliates. Mar. Biol., 108:441-447.
79. Stoecker, D. K., Michaels, A. E. & Davis, L. H. 1987. Large proportion of marine planktonic ciliates found to contain functional chloroplasts. Nature, 326:790-792.
80. Stoecker, D. K., Taniguchi, A. & Michaels, A. E. 1989. Abundance of autotrophic, mixotrophic and heterotrophic planktonic ciliates in shelf and slope waters. Mar. Ecol. Prog. Ser., 50:241-254.
81. Stoecker, D. K., Silver, M. W., Michaels, A. E. & Davis, L. H. 1988. Obligate mixotrophy in Laboea strobila, a ciliate which retains chloroplasts. Mar. Biol., 99:415-423.
82. Strüder-Kypke, M. C. & Lynn, D. H. 2003. Sequence analyses of the small subunit rRNA gene support the paraphyly of oligotrich ciliates sensu lato and support the monophyly of the subclasses Oligotrichia and Choreotrichia (Ciliophora, Spirotrichea). J. Zool., 260:87-97.
83. Suzuki, T. & Han, M.-S. 2000. A study on a new species of Tontonia (Ciliophora: Oligotrichida) from the East China Sea and adjacent sea areas. J. mar. biol. Ass. U.K., 80:989-994.
84. Swofford, D. L. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland: Sinauer Associates.
85. Tempelman, D. & Agatha, S. 1997. Biomonitoring van microzoöplankton in de Nederlandse zoute wateren 1996. TRIPOS for Rijkswaterstaat, Rijksinst. Kust en Zee, 97.T0017-1b.
86. Valbonesi, A. & Luporini, P. 1990. Description of two new species of Euplotes and Euplotes rariseta from Antarctica. Polar Biol., 11:47-53.
87. Van Goor, A. C. J. 1923. Beiträge zur Kenntnis des Nannoplanktons der südlichen Nordsee. Verh. Rapp. Rijksinst. Biol. hydrogr. Vischerejonderzoek, 1:131-182.
88. Wailes, G. H. 1943. 1. Protozoa. Canadian Pacific Fauna: 1-46.
89. Wulff, A. 1919. Ueber das Kleinplankton der Barentssee. Wiss. Meeresunters., Abt. Helgoland, 13:95-125 + Plate 1-4.