Skip to main content
SpringerLink
Log in

Protonephridia in the larvae of the paleonemertean species Carinoma mutabilis (Carinomidae, Nemertea) and Cephalothrix (Procephalothrix) filiformis (Cephalothricidae, Nemertea)

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

Abstract

During spiralian development, the first pair of nephridia forms anterior to the mouth. Each organ consists of a few cells, which is characteristic for spiralian larvae. In nemerteans, one of the unambiguously spiralian taxa, so far protonephridia, has been reported only in advanced pilidium larvae, where they likely persist as juvenile and adult nephridia. These organs have not been recorded in larvae of the basally branching nemertean taxa. In search for these organs, we examined the ultrastructure of pelagic planuliform larvae of the palaeonemerteans Carinoma mutabilis and Cephalothrix (Procephalothrix) filiformis. In both species, a pair of protonephridia is located at the level of the stomodaeum. Each protonephridium of C. mutabilis consists of two terminal cells, two duct cells and one nephropore cell, while that of C. filiformis consists of three terminal cells, three duct cells and one nephropore cell. In C. mutabilis and in C. filiformis, all terminal cells contribute to forming a compound filtration structure. In both species, the protonephridia seem to develop subepidermally, since in C. filiformis, the nephropore cells pierce the larval epidermis and in C. mutabilis, the nephropores are initially covered by the binucleated multiciliated trophoblast cells. On the fifth day, these cells degenerate, so that the protonephridium becomes functional. The occurrence of protonephridia in the larvae of both paleonemertean species is in accordance with the hypothesis that a common ancestor of Nemertea and Trochozoa had a larval stage with a pair of protonephridia. This does not contradict previous hypotheses on placing the Nemertea as an ingroup of the Trochozoa or Spiralia (= Lophotrochozoa). Whether these protonephridia are restricted to the larval phase or whether they are transformed into the adult protonephridia, like those of the pilidium larva, remains to be answered.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andrade SCS, Strand M, Schwartz M, Chen H, Kajihara H, von Döhren J, Sun S, Junoy J, Thiel M, Norenburg JL, Turbeville JM, Giribet G, Sundberg P (2011) Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea. Cladistics 28:141–159

    Article  Google Scholar 

  • Ax P (1995) Multicellular animals. Springer, Berlin

    Google Scholar 

  • Baeumler N, Haszprunar G, Ruthensteiner B (2011) Development of the excretory system in the polyplacophoran Lepidochitona corrugata: the protonephridium. J Morphol 272:972–986

    Article  PubMed  Google Scholar 

  • Bartolomaeus T (1985) Ultrastructure and development of the protonephridia of Lineus viridis (Nemertini). Microfauna Marina 2:61–83

    Google Scholar 

  • Bartolomaeus T (1989a) Ultrastructure and development of the nephridia in Anaitides mucosa (Annelida, Polychaeta). Zoomorphology 109:15–32

    Article  Google Scholar 

  • Bartolomaeus T (1989b) Larvale Nierenorgane bei Lepidochiton cinereus (Polyplacophora) und Aeolidia papillosa (Gastropoda). Zoomorphology 108:297–307

    Article  Google Scholar 

  • Bartolomaeus T (1989c) Ultrastructure and relationship between protonephridia and metanephridia in Phoronis muelleri (Phoronida). Zoomorphology 109:113–122

    Article  Google Scholar 

  • Bartolomaeus T (1993) Ultrastructure of the protonephridia in the larva of Autolytus prolifer (Annelida, Syllidae): implications for annelid phylogeny. Microfauna Marina 8:55–64

    Google Scholar 

  • Bartolomaeus T (1995) Ultrastructure of the protonephridia in larval Magelona mirabilis (Annelida, Magelonidae) and Pectinaria koreni (Annelida, Terebellida). Microfauna Marina 10:117–141

    Google Scholar 

  • Bartolomaeus T (1998) Head kidneys in hatchlings of Scoloplos armiger (Annelida: Orbiniida)—implications for the occurrence of protonephridia in lecithotrophic larvae. J Mar Biol Assoc UK 78:183–192

    Article  Google Scholar 

  • Bartolomaeus T, Ax P (1992) Protonephridia and metanephridia—their relation within the Bilateria. Zeitschrift für zoologische Systematik und Evolutionsforschung 30:21–45

    Article  Google Scholar 

  • Bartolomaeus T, Quast B (2005) Structure and development of nephridia in Annelida and related taxa. Hydrobiologia 535(536):139–165

    Article  Google Scholar 

  • Bartolomaeus T, von Döhren J (2010) Comparative morphology and evolution of the nephridia in Nemertea. J Nat Hist 44:2255–2286

    Article  Google Scholar 

  • Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749

    Article  CAS  PubMed  Google Scholar 

  • Edgecombe GD, Giribet G, Dunn CW, Hejnol A, Kristensen RM, Neves RC, Rouse GW, Worsaae K, Sørensen MV (2011) Higher level metazoan relationships: recent progress and remaining questions. Org Divers Evol 11:151–172

    Article  Google Scholar 

  • Grobe P (2007) Larval development, the origin of the coelom and the phylogenetic relationships of the Phoronida. PhD thesis, Freie Universität Berlin. http://www.diss.fu-berlin.de/diss/servlets/MCRFileNodeServlet/FUDISS_derivate_000000003523/0_author.pdf

  • Gruhl A, Wegener I, Bartolomaeus T (2009) Ultrastructure of the body cavities in Phylactolaemata (Bryozoa). J Morphol 270:306–318

    Article  PubMed  Google Scholar 

  • Haszprunar G, Ruthensteiner B (2000) Microanatomy and ultrastructure of the protonephridial system in the larva of the limpet, Patella vulgata L. (Mollusca, Patellogastropoda). J Submicrosc Cytol Pathol 32:59–67

    CAS  PubMed  Google Scholar 

  • Hay-Schmidt A (1987) The ultrastructure of the protonephridium of the actinotroch larva. Acta Zoologica 68:36–47

    Article  Google Scholar 

  • Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguna J, Bailly X, Jondelius U, Wiens M, Muller WEG, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc B 276:4261–4270

    Article  PubMed  Google Scholar 

  • Jondelius U, Ruiz-Trillo I, Baguna J, Riutort M (2002) The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zoolog Scr 31:201–215

    Article  Google Scholar 

  • Kajihara H (2007) A taxonomic catalogue of Japanese Nemerteans (Phylum Nemertea). Zoolog Sci 24:287–326

    Article  PubMed  Google Scholar 

  • Kato C (2013) Ultrastruktur der Kopfnieren (head kidneys) von sedentären Polychaten und ihre Bedeutung für die Phylogenie der Annelida. PhD thesis, University of Bonn. http://hss.ulb.uni-bonn.de/2013/3175/3175.pdf

  • Kato C, Lehrke J, Quast B (2011) Ultrastructure and phylogenetic significance of the head kidneys in Thalassema thalassemum (Thalassematinae, Echiura). Zoomorphology 130:97–106

    Article  Google Scholar 

  • Kieneke A, Ahlrichs WH, Arbizu PM, Bartolomaeus T (2008) Ultrastructure of protonephridia in Xenotrichula carolinensis syltensis and Chaetonotus maximus (Gastrotricha: Chaetonotida): comparative evaluation of the gastrotrich excretory organs. Zoomorphology 127:1–20

    Article  Google Scholar 

  • Lammert V (1985) The fine structure of protonephridia in Gnathostomulida and their comparison within Bilateria. Zoomorphology 105:308–316

    Article  Google Scholar 

  • Lüter C (1995) Ultrastructure of the metanephridia of Terebratulina retusa and Crania anomala (Brachiopoda). Zoomorphology 115:99–107

    Article  Google Scholar 

  • Lüter C (1998) Zur Ultrastruktur, Ontogenese und Phylogenie der Brachiopoda. PhD thesis. Cuvillier Verlag, Göttingen

  • Maslakova SA (2010) Development to metamorphosis of the nemertean pilidium larva. Front Zool 7:30

    Article  PubMed Central  PubMed  Google Scholar 

  • Maslakova S, von Döhren J (2009) Larval development with transitory epidermis in Paranemertess peregrina and other hoplonemerteans (phylum Nemertea). Biol Bull 216:273–292

    PubMed  Google Scholar 

  • Maslakova SA, Martindale MQ, Norenburg JL (2004) Vestigial prototroch in a basal nemertean, Carinoma tremaphoros (Nemertea; Palaeonemertea). Evol Dev 6:219–226

    Article  CAS  PubMed  Google Scholar 

  • Morris J, Nallur R, Ladurner P, Egger B, Rieger R, Hartenstein V (2004) The embryonic development of the flatworm Macrostomum sp. Dev Genes Evol 214:220–239

    Article  PubMed  Google Scholar 

  • Nielsen C (2001) Animal evolution: interrelationships of the living phyla, 2nd edn. Oxford University Press, Oxfords

    Google Scholar 

  • Nielsen C, Haszprunar G, Ruthensteiner B, Wanninger A (2007) Early development of the aplacophoran mollusc Chaetoderma. Acta Zoologica 88:231–247

    Article  Google Scholar 

  • Norenburg JL (1993) Riserius pugetensis gen. n., sp. n. (Nemertina; Anopla), a new mesopsammic species, and comments on phylogenetics of some anoplan characters. Hydrobiologia 266:203–218

    Article  Google Scholar 

  • Ruppert EE, Smith PR (1988) The functional organization of filtration nephridia. Biol Rev 171:231–258

    Article  Google Scholar 

  • Ruthensteiner B, Schaefer K (1991) On the protonephridial and ‘larval kidneys’ of Nassarius (Hinia) reticularius (Linnaeus) (Caenogastropoda). J Molluscan Stud 57:323–329

    Article  Google Scholar 

  • Ruthensteiner B, Wanninger A, Haszprunar G (2001) The protonephridial system of the tusk shell, Antalis entalis (Mollusca, Scaphopoda). Zoomorphology 121:19–26

    Article  Google Scholar 

  • Stricker SA, Reed CG, Zimmer RL (1988) The cyphonautes larva of the marine bryozoan Membranipora membranacea. II. Internal sac, musculature, and pyriform organ. Can J Zool 66:384–398

    Article  Google Scholar 

  • Sundberg P, Strand M (2007) Annulonemertes (phylum Nemertea): when segments do not count. Biol Lett 3:570–573

    Article  PubMed Central  PubMed  Google Scholar 

  • Sundberg P, Turbeville JM, Lindh S (2001) Phylogenetic relationships among higher nemertean (Nemertea) taxa inferred from 18S rDNA sequences. Mol Phylogenet Evol 20:327–334

    Article  CAS  PubMed  Google Scholar 

  • Temereva EN, Malakhov VV (2006) Development of the excretory organ in Phoronopsis harmeri (Phoronida): from protonephridium to nephromixium. Entomol Rev 86:201–209

    Article  Google Scholar 

  • Thollesson M, Norenburg JL (2003) Ribbon worm relationships: a phylogeny of the phylum Nemertea. Proc R Soc B 270:407–415

    Article  CAS  PubMed  Google Scholar 

  • Todt C, Wanninger A (2010) Of tests, trochs, shells, and spicules: development of the basal mollusk Wirenia argentea (Solenogastres) and its bearing on the evolution of trochozoan larval key features. Front Zool 7:6

    Article  PubMed Central  PubMed  Google Scholar 

  • von Dassow G, Maslakova SA (2013) How the pilidium larva pees. Integr Comp Biol 53(S1):E386–E386. http://www.sicb.org/meetings/2013/SICB%202013%20abstracts.pdf

    Google Scholar 

  • von Döhren J (2011) The fate of the larval epidermis in the Desor-larva of Lineus viridis (Pilidiophora, Nemertea) displays a historically constrained functional shift from planktotrophy to lecithotrophy. Zoomorphology 130:189–196

    Article  Google Scholar 

  • Wanninger A, Haszprunar G (2008) On the fine structure of the creeping larva of Loxosomella murmanica: additional evidence for a clade of Kamptozoa (Entoprocta) and Mollusca. Acta Zool 89:137–148

    Google Scholar 

  • Watson NA, Rohde K, Lanfranchi A (1992) The ultrastructure of the protonephridial system of Götte’s larva of Stylochus mediterraneus (Polycladida, Platyhelminthes). Zool Scripta 21:217–221

    Article  Google Scholar 

  • Wenzel C, Ehlers U, Lanfranchi A (1992) The larval protonephridium of Stylochus mediterraneus Galleni (Polycladida, Plathelminthes): an ultrastructural analysis. Microfauna Marina 7:323–340

    Google Scholar 

Download references

Acknowledgments

The study was financially supported by the German Research Council (DFG: Ba 2015/11-1). SvM was partially supported by the Friday Harbor Laboratories postdoctoral fellowship. Our thanks are due to the staff of the Friday Harbor Laboratories of the University of Washington in Friday Harbor on San Juan Island (WA, USA) and the Wadden Sea Station of the Alfred Wegener Institute for Polar and Marine Research on the Island of Sylt (Federal Republic of Germany) for their kind support. We are also grateful to two reviewers who thoroughly went through the manuscript and thus considerably improved its quality.

Author information

Authors and Affiliations

  1. Institute of Evolutionary Biology and Animal Ecology, University of Bonn, An der Immenburg 1, 53111, Bonn, Germany

    T. Bartolomaeus & J. von Döhren

  2. Oregon Institute of Marine Biology, University of Oregon, 63466 Boat Basin Road, P.O. Box 5389, Charleston, OR, 97420, USA

    S. Maslakova

Authors
  1. T. Bartolomaeus
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Maslakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. von Döhren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. Bartolomaeus.

Additional information

Communicated by A. Schmidt-Rhaesa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bartolomaeus, T., Maslakova, S. & von Döhren, J. Protonephridia in the larvae of the paleonemertean species Carinoma mutabilis (Carinomidae, Nemertea) and Cephalothrix (Procephalothrix) filiformis (Cephalothricidae, Nemertea). Zoomorphology 133, 43–57 (2014). https://doi.org/10.1007/s00435-013-0206-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-013-0206-3

Keywords

Search

Navigation