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A comprehensive and integrative re-description of Synchaeta oblonga and its relationship to Synchaeta tremula, Synchaeta rufina and Synchaeta littoralis (Rotifera: Monogononta)

  • Tanja Wilke
  • Wilko H. Ahlrichs
  • Olaf R. P. Bininda-Emonds
Original Article
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Abstract

A comprehensive re-description of the monogonont rotifer Synchaeta oblonga Ehrenberg, 1832 is presented with the aim of creating a specific and robust suite of characters to identify this species that takes account of its morphological intraspecific variability. To accomplish this, we used an integrative approach that combined morphological data of the habitus and trophi (light and scanning electron microscopy) together with ecological and molecular data to generate a data set that clearly delineates S. oblonga from the morphologically similar Synchaeta tremula (Müller, 1786) with which it is often confused. In addition, by comparing S. oblonga to all remaining members of the genus Synchaeta, we found that the literature descriptions of Synchaeta rufina Kutikova and Vasiljeva, 1982, a Lake Baikal endemic species, and Synchaeta littoralis Rousselet, 1902, a species whose taxonomic status with respect to S. oblonga had already been called into question, to both lie entirely within the range of intraspecific morphological variability present in S. oblonga. Thus, we conclude that S. oblonga can be clearly demarcated from S. tremula, but that no unambiguous morphological differences exist to delineate it from either S. rufina or S. littoralis. Because our molecular data indicate S. oblonga to be a single species despite the morphological intraspecific variability that is present, we recommend that thorough re-examinations of the taxonomic statuses of both S. rufina and S. littoralis should be performed on topotypes sampled from their type localities (Lake Baikal, Russia and Dundee, Scotland, respectively).

Keywords

Rotifera Morphology Trophi Species delimitation Synonymy Intraspecific variability 

Notes

Acknowledgments

We acknowledge Elina Kling and Janna Kling for the translation of Kutikova and Vasiljeva’s (1982) initial description of S. rufina and Backhuys Publishers for their permission to reproduce the drawings of S. rufina and S. littoralis from Hollowday (2002, p. 120, Figs. 117 and 122; p. 158, Fig. 277). We further thank Andreas Wanninger for the editorial remarks and Martin Sørensen and an anonymous reviewer whose comments and suggestions helped to improve our manuscript.

Funding

The financial support was provided by the government of Lower Saxony.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Althaus, B. (1957). Faunistisch-ökologische Studien an Rotatorien salzhaltiger Gewässer Mitteldeutschlands. (Nachtrag). Wissenschaftliche Zeitschrift der Martin-Luther-Universität Halle-Wittenberg (Sonderdruck), 6, 1–157.Google Scholar
  2. Amrén, H. (1964). Ecological and taxonomical studies on zooplankton from Spitsbergen. Zoologiska Bidrag från Uppsala, 36(2), 209–276.Google Scholar
  3. Arndt, H., Schröder, C., & Schnese, W. (1990). Rotifers of the genus Synchaeta—an important component of the zooplankton in the coastal waters of the southern Baltic. Limnologica, 21, 233–235.Google Scholar
  4. Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37–48.CrossRefGoogle Scholar
  5. Birky, C. (1964). Studies on the physiology and genetics of the rotifer, Asplanchna. I. Methods and physiology. Journal of Experimental Zoology, 155(3), 273–291.CrossRefGoogle Scholar
  6. Brownell, C. L. (1988). A new pelagic marine rotifer from the southern Benguela, Synchaeta hutchingsi, n.sp., with notes on its temperature and salinity tolerance and methods of culture. Hydrobiologia, 162, 225–233.CrossRefGoogle Scholar
  7. Buchholz, H. A. (1952). Das Brackwasserzooplankton an der schleswig-holsteinischen Ostseeküste. Christian-Albrechts-Universität Kiel.Google Scholar
  8. De Smet, W. H. (1998). Preparation of rotifer trophi for light and scanning electron microscopy. Hydrobiologia, 387, 117–121.CrossRefGoogle Scholar
  9. Dokulil, M. T., & Herzig, A. (2009). An analysis of long-term winter data on phytoplankton and zooplankton in Neusiedler See, a shallow temperate lake, Austria. Aquatic Ecology, 43(3), 715–725.CrossRefGoogle Scholar
  10. Donner, J. (1959). Bemerkungen zur Rädertierart Synchaeta oblonga EHRB. 1832. Verhandlungen der Zoologischen-Botanischen Gesellschaft Wien, 98(99), 26–30.Google Scholar
  11. Duggan, I. C., Green, J. D., & Shiel, R. J. (2002). Distribution of rotifer assemblages in North Island, New Zealand, lakes: relationships to environmental and historical factors. Freshwater Biology, 47(2), 195–206.CrossRefGoogle Scholar
  12. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797.CrossRefGoogle Scholar
  13. Ehrenberg, C. G. (1832). Über die Entwicklung und Lebensdauer der Infusionsthiere, nebst ferneren Beiträgen zu einer Vergleichung ihrer organischen Systeme. In Physikalische Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin (pp. 1–145). Berlin: Druckerei der Königlichen Akademie der Wissenschaften.Google Scholar
  14. Ehrenberg, C. G. (1834). Dritter Beitrag zur Erkenntnis großer Organisation in der Richtung des kleinsten Raumes. In Physikalische Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin (pp. 145–336). Berlin: Druckerei der Königlichen Akademie der Wissenschaften.Google Scholar
  15. Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for the am-plification of mitochondrial cytochrome c oxidase I from metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5), 294–299.PubMedGoogle Scholar
  16. Fontaneto, D., De Smet, W., & Ricci, C. (2006). Rotifers in saltwater environments, re-evaluation of an inconspicuous taxon. Journal of the Marine Biological Association of the United Kingdom, 86(4), 623–656.CrossRefGoogle Scholar
  17. Fontaneto, D., & De Smet, W. (2015). 4. Rotifera. In A. Schmidt-Rhaesa (Ed.), Handbook of zoology, Gastrotricha and Gnathifera (pp. 216–300). Berlin: De Gruyter.Google Scholar
  18. Gosse, P. H. (1887). Twenty-four new species of Rotifera. Journal of Microscopy, 7(1), 1–7.Google Scholar
  19. Gouy, M., Guindon, S., & Gascuel, O. (2010). SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27(2), 221–224.CrossRefGoogle Scholar
  20. Harring, H. K. (1921). The Rotatoria of the Canadian Arctic Expedition 1913–1918. Report of the Canadian Artic Expedition 1913–1918, Ottawa, 8, 1–23.Google Scholar
  21. Hollowday, E. D. (1949). A preliminary report on the Plymouth marine and brackish-water Rotifera. Journal of the Marine Biological Association of the United Kingdom, 28(1), 239–253.CrossRefGoogle Scholar
  22. Hollowday, E. D. (2002). Family Synchaetidae Hudson & Gosse, 1886. In H. J. F. Dumont, T. Nogrady, & H. Segers (Eds.), Rotifera. Volume 6: the Asplanchnidae, Gastropodidae, Lindiidae, Microcodinidae, Synchaetidae, Trochosphaeridae and Filinia. Guides to the identification of the microinvertebrates of the continental waters of the world (pp. 87–159). Leiden: Backhuys Publishers.Google Scholar
  23. Jersabek, C. D. & Leitner, M. F. (2013). Synchaeta littoralis Rousselet, 1902. The Rotifer World Catalog. World Wide Web electronic publication. http://rotifera.hausdernatur.at/Species/Index/1890. Accessed 10 February 2018.
  24. Jersabek, C. D., De Smet, W. H., Fischer, C., Fontaneto, D., Michaloudi, E., Wallace, R. L., & Segers, H. (2015). List of available names in zoology, candidate part Phylum Rotifera, species-group names established before 1 January 2000. 1) Completely defined names (A-list), 217 pp. and 2) incompletely defined names, with no types known (B-list). http://iczn.org/sites/iczn.org/files/LAN_CandidatePart-SpeciesRotifera-2015-12-04.pdf. Accessed 29 May 2018.
  25. Kimpel, D., Gockel, J., Gerlach, G., & Bininda-Emonds, O. R. P. (2015). Population structuring in the monogonont rotifer Synchaeta pectinata: high genetic divergence on a small geographical scale. Freshwater Biology, 60(7), 1364–1378.CrossRefGoogle Scholar
  26. Kleinow, W., Klusemann, J., & Wratil, H. (1990). A gentle method for the preparation of hard parts (trophi) of the mastax of rotifers and scanning electron microscopy of the trophi of Brachionus plicatilis (Rotifera). Zoomorphology, 109(6), 329–336.CrossRefGoogle Scholar
  27. Koste, W. (1978). Rotatoria. Die Rädertiere Mitteleuropas. Band I und II. Begründet von Max Voigt. Monogononta. Berlin: Borntraeger.Google Scholar
  28. Kutikova, L., & Vasiljeva, G. (1982). Novye I endemichnye kolovratki rodov Synchaeta i Euchlanis v faune Bajkala. Novoje O Faune Bajkala, 43–58.Google Scholar
  29. Lauterborn, R. (1894). Die pelagischen Protozoen und Rotatorien Helgolands. Wissenschaftliche Meeresuntersuchungen, 1, 207–213.Google Scholar
  30. Leigh, J. W., & Bryant, D. (2015). POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6(9), 1110–1116.CrossRefGoogle Scholar
  31. Melone, G., & Ricci, C. (1995). Rotatory apparatus in Bdelloids. Hydrobiologica, 313(1), 91–98.CrossRefGoogle Scholar
  32. Montero-Pau, J., Gómez, A., & Muñoz, J. (2008). Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic dia-pausing eggs. Limnology and Oceanography: Methods, 6(6), 218–222.Google Scholar
  33. Müller, O. F. (1786). Animalcula Infusoria fluviatilia et marina, quae detexit, systematice descripsit et ad vivum delineari curavit sistit opus hoc posthumum quod cum tabulis aeneis L. in lucem tradit vidua ejus nobilissima, cura Othonis Fabricii. Hauniae, LVI, 1–367.Google Scholar
  34. Obertegger, U., Braioni, M. G., Arrighetti, G., & Flaim, G. (2006). Trophi morphology and its usefulness for identification of formalin-preserved species of Synchaeta Ehrenberg, 1832 (Rotifera: Monogononta: Synchaetidae). Zoologischer Anzeiger, 245(2), 109–120.CrossRefGoogle Scholar
  35. Pejler, B. (1957). On variation and evolution in planktonic Rotatoria. Zoologiska Bidrag från Uppsala, 32, 1–66.Google Scholar
  36. Pontin, R. M. (1978). A key to the freshwater planktonic and semi-planktonic Rotifera of the British Isles. Ambleside: Freshwater Biological Association.Google Scholar
  37. Pourriot, R. (1965). Notes taxonomiques sur quelques Rotiféres planctoniques. Hydrobiologia, 26(3/4), 579–604.CrossRefGoogle Scholar
  38. Raupach, M. J., Mayer, C., Malyutina, M., & Wägele, J. W. (2009). Multiple origins of deep-sea Asellota (Crustacea: Isopoda) from shallow waters revealed by molecular data. Proceedings of the Royal Society of London, Series B: Biological Sciences, 276(1658), 799–808.CrossRefGoogle Scholar
  39. Raupach, M. J., Astrin, J. J., Hannig, K., Peters, M. K., Stoeckle, M. Y., & Wägele, J. W. (2010). Molecular species identification of Central European ground beetles (Coleoptera: Car-abidae) using nuclear rDNA expansion segments and DNA barcodes. Frontiers in Zoology, 7(1), 26.CrossRefGoogle Scholar
  40. Remane, A. (1929). Rotatoria. In G. Grimpe (Ed.), Die Tierwelt der Nord- und Ostsee (pp. 1–156). Leipzig: Akademische Verlagsgesellschaft.Google Scholar
  41. Rousselet, C. (1902). The genus Synchaeta: a monographic study, with descriptions of five new species. Journal of Microscopy, 22(4), 393–411.Google Scholar
  42. Rozanska, Z. (1963). Zooplankton Zalewu Wislanego. Zeszyty Naukowe Wysej Szkoly Rolniczej w Olsztynie, 16(278), 41–57.Google Scholar
  43. Ruttner-Kolisko, A. (1972). Rotatoria. In H. J. Elster & W. Ohle (Eds.), Die Binnengewässer, Bd. 26. Das Zooplankton der Binnengewässer. 1. Teil (pp. 99–234). Stuttgart: Schweizerbart’sche Verlagsbuchhandlung.Google Scholar
  44. Sheveleva, N. G., Pomazkova, G. I., & Melnik, N. G. (1995). Eco-taxonomical review of Rotatoria, Cladocera, Calanoida and Cyclopoida of Lake Baikal. Japanese Journal of Limnology, 56(1), 49–62.CrossRefGoogle Scholar
  45. Shiel, R. J., & Koste, W. (1993). Rotifera from Australian inland waters. IX. Gastropodidae, Synchaetidae, Asplanchnidae (Rotifera: Monogononta). Transactions of the Royal Society of South Australia, 117(3), 111–139.Google Scholar
  46. Segers, H. (2004). Rotifera: Monogononta. In C. M. Yule & H. S. Yong (Eds.), Freshwater invertebrates of the Malaysian region (pp. 106–120). Kuala Lumpur: Academy of Sciences of Malaysia and Monash University.Google Scholar
  47. Segers, H. (2007). Annotated checklist of the rotifers (phylum Rotifera), with notes on no-menclature, taxonomy and distribution. Zootaxa, 1564, 1–104.Google Scholar
  48. Smirnov, N. S. (1933). Rotatorien, gesammelt während der Expeditionen auf den Dampfern ‘Sedow’1930 und ‘Lomonossow’1931. Transactions of the Arctic Institute Leningrad, 8, 79–91.Google Scholar
  49. Smith, J. C. (1904). Synchaeta bicornis: a new rotifer from the brackish waters of Lake Pontchartrain, Louisiana. Transactions of the American Microscopical Society, 25, 121–126.CrossRefGoogle Scholar
  50. Stemberger, R. S., & Gilbert, J. J. (1985). Body size, food concentration, and population growth in planktonic rotifers. Ecology, 66(4), 1151–1159.CrossRefGoogle Scholar
  51. Telesh, I., & Heerkloss, H. (2002). Atlas of estuarine zooplankton of the southern and eastern Baltic Sea. Part 1: Rotifera. Hamburg: Verlag Dr. Kovac̆.Google Scholar
  52. Voigt, M. (1956–1957). Rotatoria. Die Rädertiere Mitteleuropas. I Textband, II Tafelband. Berlin: Borntraeger.Google Scholar
  53. Wærvågen, S. B., & Andersen, T. (2017). Seasonal quantitative dynamics and ecology of pelagic rotifers in an acidified boreal lake. Journal of Limnology, 77(1), 147–160.CrossRefGoogle Scholar
  54. Wierzejski, A. (1893). Rotatoria (wrotki) Galicyi. Rozprawy Akademii Umiejętności w Krakowie. Wydział Matematyczno-Przyrodniczy, 6, 160–265.Google Scholar
  55. Wilke, T., Ahlrichs, W. H., & Bininda-Emonds, O. R. P. (2017). A comprehensive and integrative re-description of Synchaeta tremula (Müller, 1786) and the newly rediscovered Synchaeta tremuloida Pourriot, 1965 (Rotifera: Synchaetidae). Zootaxa, 4276(4), 503–518.CrossRefGoogle Scholar
  56. Wilke, T., Ahlrichs, W. H., & Bininda-Emonds, O. R. P. (2018). On the importance of robust species descriptions for Rotifera: re-descriptions of Synchaeta stylata and Synchaeta longipes and a comparison to Synchaeta jollyae. Zoologischer Anzeiger., 277, 42–54.CrossRefGoogle Scholar
  57. Zeng, L., Liu, B., Dai, Z., Zhou, Q., Kong, L., Zhang, Y., He, F., & Wu, Z. (2017). Analyzing the effects of four submerged macrophytes with two contrasting architectures on zooplankton: a mesocosm experiment. Journal of Limnology, 76(3), 581–590.Google Scholar
  58. Zimmermann-Timm, H., Holst, H., & Kausch, H. (2007). Spatial dynamics of rotifers in a large lowland river, the Elbe, Germany: how important are retentive shoreline habitats for the plankton community? Hydrobiologia, 593(1), 49–58.CrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2018

Authors and Affiliations

  • Tanja Wilke
    • 1
  • Wilko H. Ahlrichs
    • 1
  • Olaf R. P. Bininda-Emonds
    • 1
  1. 1.AG Systematik und Evolutionsbiologie, Institut für Biologie und Umweltwissenschaften (IBU)Carl von Ossietzky Universität OldenburgOldenburgGermany

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