Zoomorphology

, Volume 127, Issue 1, pp 1–20 | Cite as

Ultrastructure of protonephridia in Xenotrichula carolinensis syltensis and Chaetonotus maximus (Gastrotricha: Chaetonotida): comparative evaluation of the gastrotrich excretory organs

  • Alexander Kieneke
  • Wilko H. Ahlrichs
  • Pedro Martínez Arbizu
  • Thomas Bartolomaeus
Original Paper

Abstract

In an attempt to obtain detailed information on the entire protonephridial system in Gastrotricha, we have studied the protonephridial ultrastructure of two paucitubulatan species, Xenotrichula carolinensis syltensis and Chaetonotus maximus by means of complete sets of ultrathin sections. In spite of some differences in detail, the morphology of protonephridia in both examined species shows a common pattern: Both species have one pair of protonephridia that consist of a bicellular terminal organ, a voluminous, aciliar canal cell and an adjacent, aciliar nephridiopore cell. The terminal organ consists of two monociliar terminal cells each with a distal cytoplasmic lobe. These lobes interdigitate and surround cilia and microvilli of the terminal cells. Where both lobes interdigitate, a meandering cleft is formed that is covered by the filtration barrier. We here term the entire structure composite filter. The elongated, in some regions convoluted protonephridial lumen opens distally to the outside via a permanent nephridiopore. A comparison with the protonephridia of other species of the Gastrotricha allows hypothesising the following autapomorphies of the Paucitubulata: The bicellular terminal organ with a composite filter, the convoluted distal canal cell lumen and the absence of cilia, ciliary basal structures and microvilli within the canal cell. Moreover, this comparative survey could confirm important characteristics of the protonephridial system assumed for the ground pattern of Gastrotricha like, for example, the single terminal cell with one cilium surrounded by eight microvilli.

Keywords

Gastrotricha Paucitubulata Phylogenetic implications Protonephridial system Ultrastructure 

References

  1. Ax P (2003) Multicellular animals. Order in nature—System made by man. Vol. III. Springer, BerlinGoogle Scholar
  2. Balsamo M, Todaro MA (2002) Gastrotricha. In: Rundle SD, Robertson AL, Schmid-Araya JM (eds) Freshwater meiofauna: biology and ecology. Backhuys Publishers, Leiden, pp 45–61Google Scholar
  3. Bartolomaeus T, Ax P (1992) Protonephridia and metanephridia–their relation within the Bilateria. Z Zool Syst Evol Forsch 30:21–45CrossRefGoogle Scholar
  4. Brandenburg J (1962) Elektronenmikroskopische Untersuchung des Terminal-apparates von Chaetonotus sp. (Gastrotrichen) als ersten Beispiels einer Cyrtocyte bei Askhelminthen. Z Zellforsch 57:136–144CrossRefGoogle Scholar
  5. d’Hondt J-L (1971) Gastrotricha. Oceanogr Mar Biol Ann Rev 9:141–192Google Scholar
  6. Ehlers U, Ahlrichs W, Lemburg C, Schmidt-Rhaesa A (1996) Phylogenetic systematisation of the Nemathelminthes (Aschelminthes). Verh Dtsch Zool Ges 89.1:8Google Scholar
  7. Ehrenberg CJ (1831) Organisation systematik und geographisches verhältnis der Infusionstierchen. Dümmler, BerlinGoogle Scholar
  8. Fischer U (1994) Additional aspects to the protonephridial system of Dactylopodola baltica (Gastrotricha, Macrodasyida). Microfauna Mar 9:285–289Google Scholar
  9. Giribet G, Distel DL, Polz M, Sterrer W, Wheeler WC (2000) Triploblastic relationships with emphasis on the Acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology. Syst Biol 49(3):539–562PubMedCrossRefGoogle Scholar
  10. Hochberg R, Litvaitis MK (2000) Phylogeny of Gastrotricha: a morphology-based framework of Gastrotrich relationships. Biol Bull 198:299–305PubMedCrossRefGoogle Scholar
  11. Hochberg R, Litvaitis MK (2001) Macrodasyida (Gastrotricha): a cladistic analysis of morphology. Invertebr Biol 120:124–135CrossRefGoogle Scholar
  12. Kristensen RM, Hay-Schmidt A (1989) The protonephridia of the Arctic Kinorhynch Echinoderes aquilonius (Cyclorhagida, Echinoderidae). Acta Zool 70.1:13–27Google Scholar
  13. Manylov OG, Vladychenskaya NS, Milyutina IA, Kedrova OS, Korokhov NP, Dvoryanchikov GA, Aleshin VA, Petrov NB (2004) Analysis of 18S rRNA gene sequences suggests significant molecular differences between Macrodasyida and Chaetonotida (Gastrotricha). Mol Phylogenet Evol 30.3:850–854CrossRefGoogle Scholar
  14. Marotta R, Guidi L, Pierboni L, Ferraguti M, Todaro MA, Balsamo M (2005) Sperm ultrastructure of Macrodasys caudatus (Gastrotricha: Macrodasyida) and a sperm-based phylogenetic analysis of Gastrotricha. Meiofauna Marina 14:9–21Google Scholar
  15. Mock H (1979) Chaetonotoidea (Gastrotricha) der Nordseeinsel Sylt. Mikrofauna Meeresboden 78:1–107Google Scholar
  16. Neuhaus B (1987) Ultrastructure of the protonephridia in Dactylopodola baltica and Mesodasys laticaudatus (Macrodasyida): implications for the ground pattern of the Gastrotricha. Microfauna Mar 3:419–438Google Scholar
  17. Remane A (1936) Gastrotricha und Kinorhyncha. In: Bronn HG (ed) Klassen und Ordnungen des Tierreichs. 4. Band, II. Abteilung, 1. Buch, 2. Teil. Akademische Verlagsgesellschaft, Leipzig, pp 1–242Google Scholar
  18. Ruppert EE (1972) An efficient, quantitative method for sampling the Meiobenthos. Limnol Oceanogr 17:629–631CrossRefGoogle Scholar
  19. Ruppert EE (1979) Morphology and systematics of the Xenotrichulidae (Gastrotricha, Chaetonotida). Mikrofauna des Meeresbodens 76:1–56Google Scholar
  20. Ruppert EE (1982) Comparative ultrastructure of the Geastrotrich Pharynx and the evolution of myoepithelial foreguts in Aschelminthes. Zoomorphology 99:181–220CrossRefGoogle Scholar
  21. Ruppert EE (1991) Gastrotricha. In: Harrison FW, Ruppert EE (eds) Microscopic Anatomy of Invertebrates. Vol. 4, Aschelminthes. Wiley-Liss, New York, pp 41–109Google Scholar
  22. Ruppert EE, Smith PR (1988) The functional organisation of filtration Nephridia. Biol Rev 63:231–258Google Scholar
  23. Schmidt-Rhaesa A, Bartolomaeus T, Lemburg C, Ehlers U, Garey JR (1998) The position of the Arthropoda in the phylogenetic system. J Morphol 238:263–285CrossRefGoogle Scholar
  24. Teuchert G (1967) Zum Protonephridialsystem mariner Gastrotrichen der Ordnung Macrodasyoidea. Marine Biol 1:110–112CrossRefGoogle Scholar
  25. Teuchert G (1973) Die Feinstruktur des Protonephridialsystems von Turbanella cornuta Remane, einem marinen Gastrotrich der Ordnung Macrodasyoidea. Z Zellforsch 136:277–289PubMedCrossRefGoogle Scholar
  26. Todaro MA, Littlewood DTJ, Balsamo M, Herniou EA, Cassanello S, Manicardi G, Wirz A, Tongiorgi P (2003) The interrelationships of the Gastrotricha using nuclear small rRNA subunit sequence data, with an interpretation based on morphology. Zool Anz 242:145–156CrossRefGoogle Scholar
  27. Todaro MA, Balsamo M, Kristensen RM (2005) A new genus of marine chaetonotids (Gastrotricha), with a description of two new species from Greenland and Denmark. J Mar Biol Ass UK 85:1391–1400CrossRefGoogle Scholar
  28. Travis PB (1983) Ultrastructural study of body wall organization and Y-cell composition in the Gastrotricha. Z Zool Syst Evol Forsch 21:52–68CrossRefGoogle Scholar
  29. Uhlig G (1964) Eine einfache Methode zur Extraktion der vagilen, mesopsammalen Mikrofauna. Helgoländer Wiss Meeresunters 11:178–185CrossRefGoogle Scholar
  30. Wilke U (1954) Mediterrane gastrotrichen. Zool Jb Abt Syst 82:497–550Google Scholar
  31. Zelinka K (1889) Die Gastrotrichen. Eine monographische Darstellung ihrer Anatomie, Biologie und Systematik. Z wiss Zool 49:209–384Google Scholar
  32. Zrzavý J (2003) Gastrotricha and metazoan phylogeny. Zool Scr 32:61–81CrossRefGoogle Scholar
  33. Zrzavý J, Mihulka S, Kepka P, Bezdek A, Tietz D (1998) Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics 14:249–285Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Alexander Kieneke
    • 1
    • 2
  • Wilko H. Ahlrichs
    • 1
  • Pedro Martínez Arbizu
    • 2
  • Thomas Bartolomaeus
    • 3
  1. 1.Zoosystematik & Morphologie, Institut für Biologie und UmweltwissenschaftenCarl von Ossietzky Universität OldenburgOldenburgGermany
  2. 2.Forschungsinstitut Senckenberg, DZMBWilhelmshavenGermany
  3. 3.Evolution und Systematik der Tiere, FU BerlinBerlinGermany

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