Skip to main content

Advertisement

Log in

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

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Ax P (2003) Multicellular animals. Order in nature—System made by man. Vol. III. Springer, Berlin

    Google Scholar 

  • Balsamo M, Todaro MA (2002) Gastrotricha. In: Rundle SD, Robertson AL, Schmid-Araya JM (eds) Freshwater meiofauna: biology and ecology. Backhuys Publishers, Leiden, pp 45–61

    Google Scholar 

  • Bartolomaeus T, Ax P (1992) Protonephridia and metanephridia–their relation within the Bilateria. Z Zool Syst Evol Forsch 30:21–45

    Article  Google Scholar 

  • Brandenburg J (1962) Elektronenmikroskopische Untersuchung des Terminal-apparates von Chaetonotus sp. (Gastrotrichen) als ersten Beispiels einer Cyrtocyte bei Askhelminthen. Z Zellforsch 57:136–144

    Article  Google Scholar 

  • d’Hondt J-L (1971) Gastrotricha. Oceanogr Mar Biol Ann Rev 9:141–192

    Google Scholar 

  • Ehlers U, Ahlrichs W, Lemburg C, Schmidt-Rhaesa A (1996) Phylogenetic systematisation of the Nemathelminthes (Aschelminthes). Verh Dtsch Zool Ges 89.1:8

    Google Scholar 

  • Ehrenberg CJ (1831) Organisation systematik und geographisches verhältnis der Infusionstierchen. Dümmler, Berlin

  • Fischer U (1994) Additional aspects to the protonephridial system of Dactylopodola baltica (Gastrotricha, Macrodasyida). Microfauna Mar 9:285–289

    Google Scholar 

  • 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):539–562

    Article  PubMed  CAS  Google Scholar 

  • Hochberg R, Litvaitis MK (2000) Phylogeny of Gastrotricha: a morphology-based framework of Gastrotrich relationships. Biol Bull 198:299–305

    Article  PubMed  CAS  Google Scholar 

  • Hochberg R, Litvaitis MK (2001) Macrodasyida (Gastrotricha): a cladistic analysis of morphology. Invertebr Biol 120:124–135

    Article  Google Scholar 

  • Kristensen RM, Hay-Schmidt A (1989) The protonephridia of the Arctic Kinorhynch Echinoderes aquilonius (Cyclorhagida, Echinoderidae). Acta Zool 70.1:13–27

    Google Scholar 

  • 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 30.3:850–854

    Article  CAS  Google Scholar 

  • 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 14:9–21

    Google Scholar 

  • Mock H (1979) Chaetonotoidea (Gastrotricha) der Nordseeinsel Sylt. Mikrofauna Meeresboden 78:1–107

    Google Scholar 

  • Neuhaus B (1987) Ultrastructure of the protonephridia in Dactylopodola baltica and Mesodasys laticaudatus (Macrodasyida): implications for the ground pattern of the Gastrotricha. Microfauna Mar 3:419–438

    Google Scholar 

  • 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 1–242

    Google Scholar 

  • Ruppert EE (1972) An efficient, quantitative method for sampling the Meiobenthos. Limnol Oceanogr 17:629–631

    Article  Google Scholar 

  • Ruppert EE (1979) Morphology and systematics of the Xenotrichulidae (Gastrotricha, Chaetonotida). Mikrofauna des Meeresbodens 76:1–56

    Google Scholar 

  • Ruppert EE (1982) Comparative ultrastructure of the Geastrotrich Pharynx and the evolution of myoepithelial foreguts in Aschelminthes. Zoomorphology 99:181–220

    Article  Google Scholar 

  • Ruppert EE (1991) Gastrotricha. In: Harrison FW, Ruppert EE (eds) Microscopic Anatomy of Invertebrates. Vol. 4, Aschelminthes. Wiley-Liss, New York, pp 41–109

    Google Scholar 

  • Ruppert EE, Smith PR (1988) The functional organisation of filtration Nephridia. Biol Rev 63:231–258

    Google Scholar 

  • Schmidt-Rhaesa A, Bartolomaeus T, Lemburg C, Ehlers U, Garey JR (1998) The position of the Arthropoda in the phylogenetic system. J Morphol 238:263–285

    Article  Google Scholar 

  • Teuchert G (1967) Zum Protonephridialsystem mariner Gastrotrichen der Ordnung Macrodasyoidea. Marine Biol 1:110–112

    Article  Google Scholar 

  • Teuchert G (1973) Die Feinstruktur des Protonephridialsystems von Turbanella cornuta Remane, einem marinen Gastrotrich der Ordnung Macrodasyoidea. Z Zellforsch 136:277–289

    Article  PubMed  CAS  Google Scholar 

  • 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 242:145–156

    Article  Google Scholar 

  • 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 85:1391–1400

    Article  Google Scholar 

  • Travis PB (1983) Ultrastructural study of body wall organization and Y-cell composition in the Gastrotricha. Z Zool Syst Evol Forsch 21:52–68

    Article  Google Scholar 

  • Uhlig G (1964) Eine einfache Methode zur Extraktion der vagilen, mesopsammalen Mikrofauna. Helgoländer Wiss Meeresunters 11:178–185

    Article  Google Scholar 

  • Wilke U (1954) Mediterrane gastrotrichen. Zool Jb Abt Syst 82:497–550

    Google Scholar 

  • Zelinka K (1889) Die Gastrotrichen. Eine monographische Darstellung ihrer Anatomie, Biologie und Systematik. Z wiss Zool 49:209–384

    Google Scholar 

  • Zrzavý J (2003) Gastrotricha and metazoan phylogeny. Zool Scr 32:61–81

    Article  Google Scholar 

  • Zrzavý J, Mihulka S, Kepka P, Bezdek A, Tietz D (1998) Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics 14:249–285

    Google Scholar 

Download references

Acknowledgements

We greatly appreciate the hospitality of the Wadden Sea Station in List/Sylt (Alfred Wegener Institute, AWI) and its staff, who made possible a fruitful stay for collecting marine gastrotrichs. Additionally, we acknowledge PD Dr. Andreas Schmidt-Rhaesa for invaluable pieces of advice in the early stages of this project. This research was funded by the German Science Foundation (DFG) through a research grant (AH 94/3-1 and -2, MA 2557/4-1 and -2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexander Kieneke.

Additional information

Communicated by G. Steiner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kieneke, A., Ahlrichs, W.H., Martínez Arbizu, P. et al. Ultrastructure of protonephridia in Xenotrichula carolinensis syltensis and Chaetonotus maximus (Gastrotricha: Chaetonotida): comparative evaluation of the gastrotrich excretory organs. Zoomorphology 127, 1–20 (2008). https://doi.org/10.1007/s00435-007-0051-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-007-0051-3

Keywords

Navigation