Skip to main content
Log in

Male genital organs in the eulittoral meiofaunal polychaete Stygocapitella subterranea (Annelida, Parergodrilidae): ultrastructure, functional and phylogenetic significance

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

Abstract

The marine interstitial polychaete Stygocapitella subterranea is characterized by aberrant morphological and biological traits resembling those of clitellates and Hrabeiella periglandulata, a terrestrial polychaete species. Although clearly related to the terrestrial Parergodrilus heideri, there are distinct differences in their morphology. An ultrastructural study of the male genital organs was undertaken to look for common apomorphic features in Parergodrilidae, to find structural evidence for clarifying their reproductive biology and mode of sperm transfer. Finally it should be elucidated whether a supposed sister-group relationship of Parergodrilidae and Orbiniidae based on molecular evidence can be supported by morphological characters as well. In S. subterranea the male organs consist of an unpaired seminal vesicle, a pair of sperm ducts and two large tube-like prostate glands. These glands constitute the distal parts of the gonoducts and open ventrally on a small genital papilla in chaetiger 9. True copulatory organs or organs for storage of mature sperm are lacking. The seminal vesicle is a coelomic cavity composed of two apposed coelomic linings supplied with blood spaces. The testes are found ventrally. The prostate glands are covered by a single layer of muscle fibres running in a longitudinal/spiral direction along the gland. There are no signs of spermatophore formation in any part of the male system. Since females always carry sperm, pseudocopulation can be excluded and the likelihood of either direct transfer of sperm or hypodermic injection is discussed. The structure of genital organs reveals similarities to those of P. heideri. Gonochorism, paired seminal vesicles and two pairs of male gonoducts opening in chaetigers 9 and 10 with a distal glandular part most likely belong to the ground pattern of Parergodrilidae. The observations confirm that consistencies with either clitellates or H. periglandulata are the result of convergent evolutionary events. On the other hand, the relationship of Parergodrilidae to an orbiniid/questid clade receives support from the present data.

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

Similar content being viewed by others

References

  • Anderson DT (1959) The embryology of the polychaete Scoloplos armiger. Q J Microsc Sci 100:89–166

    Google Scholar 

  • Blake J (2000) A new genus and species of polychaete worm (Family Orbiniidae) from methane seeps in the Gulf of Mexico, with a review of the systematics and phylogenetic interrelationships of the genera of Orbiniidae. Cah Biol Mar 41:435–449

    Google Scholar 

  • Bleidorn C (2007) The role of character loss in phylogenetic reconstruction as exemplified for the Annelida. J Zool Syst Evol Res doi:10.1111/j.1439–0469.2007.00425.x:1–9

  • Bleidorn C (2005) Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta) based on molecular data. Zool J Linn Soc 144:59–73

    Article  Google Scholar 

  • Bleidorn C, Vogt L, Bartolomaeus T (2003) New insights into polychaete phylogeny (Annelida) inferred from 18S rDNA sequences. Mol Phyl Evol 29:279–288

    Article  CAS  Google Scholar 

  • Brinkhurst RO (1982) Evolution in the Annelida. Can J Zool 60:1043–1059

    Article  Google Scholar 

  • Bührmann C, Westheide W, Purschke G (1996) Ultrastructure of the genital organs in the interstitial syllid Petitia amphophthalma (Annelida, Polychaeta). Acta Zool (Stockh) 77:201–211

    Google Scholar 

  • Eisig H (1914) Zur Systematik, Anatomie und Morphologie der Ariciiden nebst Beiträgen zur generellen Systematik. Mitt zool St Neapel 21:153–593

    Google Scholar 

  • Ermack TH, Eakin RM (1976) Fine structure of the cerebral and pygidial ocelli in Chone ecaudata (Polychaeta: Sabellidae). J Ultrastruct Res 54:243–260

    Article  Google Scholar 

  • Erséus C (1987) Phylogenetic analysis of the aquatic Oligochaeta under the principle of parsimony. Hydrobiologia 155:75–89

    Article  Google Scholar 

  • Erséus C (2005) Phylogeny of oligochaetous Clitellata. Hydrobiologia 535/536:357–372

    Article  CAS  Google Scholar 

  • Erséus C Källersjö M (2004) 18S rDNA phylogeny of Clitellata (Annelida). Zool Scr 33:187–196

    Article  Google Scholar 

  • Giere OW, Riser NW (1981) Questidae—polychaetes with oligochaetoid morphology and development. Zool Scr 10:95–103

    Article  Google Scholar 

  • Giere OW, Erséus C (1998) A systematic account of the Questidae (Annelida, Polychaeta), with description of new taxa. Zool Scr 27:345–360

    Article  Google Scholar 

  • Glasby CJ (2000) Family Orbiniidae. In: Beesly PL, Ross GJB, Glasby CJ (eds) Polychaetes and allies: the southern synthesis. Fauna of Australia. Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula, vol 4A. CISRO Publishing, Melbourne, pp 79–82

    Google Scholar 

  • Jamieson BGM, Rouse GW (1989) The spermatozoa of the Polychaeta (Annelida): an ultrastructural review. Biol Rev 64:93–157

    PubMed  CAS  Google Scholar 

  • Jamieson BGM, Ferraguti M (2005) Non-leech Clitellata. In: Rouse G, Pleijel F (eds) Reproductive biology and phylogeny of Annelida. Science Publishers, Enfield, pp 235–392

    Google Scholar 

  • Jördens J, Struck T, Purschke G (2004) Phylogenetic interference regarding Parergodrilidae and Hrabeiella periglandulata (“Polychaeta”, Annelida) based on 18S rDNA, 28S rDNA and COI sequences. J Zool Syst Evol Res 42:270–280

    Article  Google Scholar 

  • Karling TG (1958) Zur Kenntnis von Stygocapitella subterranea Knöllner und Parergodrilus heideri Reisinger (Annelida). Ark Zool Stockh 11:307–342

    Google Scholar 

  • Knöllner F (1934) Die Tierwelt des Küstengrundwassers bei Schilksee (Kieler Bucht) V. Stypocapitella [sic] subterranea nov. gen. nov. spec. Schr naturw Ver Schl-Holst 20:468–472

  • Kuper M, Westheide W (1997) Ultrastructure of the male reproductive organs in the interstitial annelid Sphaerosyllis hermaphrodita (“Polychaeta”, Syllidae) Zoomorphology 117:13–22

    Article  Google Scholar 

  • Müller, MC (1999) Das Nervensystem der Polychaeten: Immunhistochemische Untersuchungen an ausgewählten Taxa. Ph.D. Thesis, Universität Osnabrück, pp 1–402

  • Pizl V, Chalupsky J (1984) Hrabeiella periglandulata gen. et sp. n. (Annelida)—a curious worm from Czechoslowakia. Vest cs Spolec zool 48:291–295

    Google Scholar 

  • Purschke G (1987) Anatomy and ultrastructure of ventral pharyngeal organs and their phylogenetic importance in Polychaeta (Annelida). III. The pharynx of the Parergodrilidae. Zool Jb Anat 115:331–362

    Google Scholar 

  • Purschke G (1988) Anatomy and ultrastructure of ventral pharyngeal organs and their phylogenetic importance in Polychaeta (Annelida). V. The pharynges of the Ctenodrilidae and Orbiniidae. Zoomorphology 108:119–135

    Article  Google Scholar 

  • Purschke G (1999) Terrestrial polychaetes—models for the evolution of the Clitellata (Annelida)? Hydrobiologia 406:87–99

    Article  Google Scholar 

  • Purschke G (2002) Male genital organs, spermatogenesis and spermatozoa in the enigmatic terrestrial polychaete Parergodrilus heideri (Annelida, Parergodrilidae) Zoomorphology 121:125–138

    Article  Google Scholar 

  • Purschke G (2005) Problematic annelid groups. In: Rouse G, Pleijel F (eds) Reproductive biology and phylogeny of Annelida, Science Publishers, Enfield, pp 639–667

    Google Scholar 

  • Purschke G, Fursman MC (2005) Spermatogenesis and spermatozoa in Stygocapitella subterranea (Annelida, Parergodrilidae), an enigmatic supralittoral polychaete. Zoomorphology 124:137–148

    Article  Google Scholar 

  • Purschke G, Tzetlin AB (1996) Dorsolateral folds in the polychaete foregut: structure, prevalence and phylogenetic significance. Acta Zool (Stockh) 77:33–49

    Article  Google Scholar 

  • Purschke G, Westheide W, Rhode D, Brinkhurst RO (1993) Morphological reinvestigation and phylogenetic relationship of Acanthobdella peledina (Annelida, Clitellata) Zoomorphology 113:91–101

    Article  Google Scholar 

  • Reisinger E (1925) Ein landbewohnender Archiannelide—zugleich ein Beitrag zur Systematik der Archianneliden. Z Morphol Ökol Tiere 3:197–254

    Article  Google Scholar 

  • Reisinger E (1960) Die Lösung des Parergodrilus-Problems. Z Morphol 48:517–544

    Google Scholar 

  • Rice SA (1992) Polychaeta: spermatogenesis and spermiogenesis. In: Harrison FW (eds) Microscopic anatomy of invertebrates, vol 7. Wiley, New York, pp 129–151

    Google Scholar 

  • Rota E (1998) Morphology and adaptations of Parergodrilus Reisinger and Hrabeiella Pizl & Chalupsky, two enigmatic soil-dwelling annelids. Ital J Zool 65:75–84

    Article  Google Scholar 

  • Rota E, Lupetti P (1997) An ultrstructural investigation of Hrabeiella Pizl & Chalupsky, 1984 (Annelida). II. The spermatozoon. Tiss Cell 29:603–609

    Article  CAS  Google Scholar 

  • Rota E, Martin P, Erséus C (2001) Soil-dwelling polychaetes: enigmatic as ever? Some hints on their phylogenetic relationships as suggested by a maximum parsimony analysis of 18S rRNA sequences. Contr Zool 70:127–138

    Google Scholar 

  • Rouse GW (2005) Annelid sperm and spermiogenesis. In: Rouse G, Pleijel F (eds) Reproductive biology and phylogeny of Annelida, Science Publishers, Enfield, pp 45–76

    Google Scholar 

  • Rouse GW, Pleijel F (2001) Polychaetes. Oxford University, Oxford, pp 1–354

    Google Scholar 

  • Sawyer RT (1986) Leech biology and behaviour. I. Anatomy, physiology and behaviour. Clarendon, Oxford, pp 1–418

    Google Scholar 

  • Schmidt H, Westheide W (2000) Are the meiofaunal polychaetes Hesionides arenaria and Stygocapitella subterranea true cosmopolitan species?—results from RAPD-PCR investigations. Zool Scr 29:17–27

    Article  Google Scholar 

  • Struck TH, Purschke G (2005) The sister group relationship of Aeolosomatidae and Potamodrilidae (Annelida: “Polychaeta”)—a molecular phylogenetic approach based on 18S rDNA and cytochrome oxidase I. Zool Anz 243:281–293

    Article  Google Scholar 

  • Struck T, Hessling R, Purschke G (2002) The phylogenetic position of Aeolosomatidae and Parergodrilidae, two enigmatic oligochaete-like taxa of the “Polychaeta”, based on molecular data from 18S rDNA sequences. J Zool Syst Evol Res 40:155–163

    Article  Google Scholar 

  • Struck TH, Purschke G, Halanych KM (2005) A scaleless scale worm: molecular evidence for the phylogenetic placement of Pisione remota (Pisionidae Annelida). Mar Biol Res 1:243–253

    Article  Google Scholar 

  • Struck TH, Halanych KM, Purschke G (2005) Dinophilidae (Annelida) is most likely not a progenetic Eunicida: evidence from 18S and 28S rDNA. Mol Phyl Evol 37:619–623

    Article  CAS  Google Scholar 

  • Tzetlin A, Purschke G (2005) Pharynx and intestine In: Bartolomaeus T, Purschke G (eds) Morphology, molecules, evolution and phylogeny in polychaeta and related taxa. Hydrobiologia 535/536:199–225

  • Westheide W (1982) Ultrastructure of the genital organs in interstitial polychaetes. III. Penes and ejaculatory ducts in Hesionides arenaria (Hesionidae). Helgoländer Meeresunters 35:479–488

    Article  Google Scholar 

  • Westheide W (1984) The concept of reproduction in polychaetes with small body size: adaptations in interstitial species. In: Fischer A, Pfannenstiel H-D (eds) Polychaete reproduction. Fortschr Zool 29:265–287

  • Westheide W (1987) Progenesis as a principle in meiofauna evolution. J Nat Hist 21:843–854

    Article  Google Scholar 

  • Westheide W (1988) Genital organs. In: Westheide W, Hermans CO (eds) The ultrastructure of Polychaeta. Microfauna marina 4:263–279

  • Westheide W (1990) Polychaetes: interstitial families. In: Kermack DM, Barnes RSK (eds) Synopsis of the British fauna, vol 44. Universal Book Services/Backhuys, Oestgeest, pp 1–152

    Google Scholar 

  • Westheide W, Purschke G (1988) Organism processing. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution, Washington, pp 146–160

    Google Scholar 

  • Westheide W, Purschke G, Mangerich W (1994) Sinohesione genitaliphora gen. et sp. n. (Polychaeta, Hesionidae), an interstitial annelid with unique genital organs. Zool Scr 23:95–105

    Article  Google Scholar 

  • Worsaae K, Nygren A, Rouse GW, Giribet G, Persson J, Sundberg P, Pleijel F (2005) Phylogenetic position of Nerillidae and Aberranta (Polychaeta, Annelida), analysed by direct optimization of combined molecular and morphological data. Zool Scr 34:313–328

    Article  Google Scholar 

Download references

Acknowledgments

We are indebted to Professor Dr. W. Westheide for valuable discussions. Various kinds of support by the head of the zoology department, Professor Dr. A. Paululat, is gratefully acknowledged. Thanks are due to Anna Stein, Mechthild Krabusch and Werner Mangerich for technical assistance. The study was supported by a grant from the Deutsche Forschungsgemeinschaft, DFG.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Günter Purschke.

Additional information

This paper is dedicated to our scientific teacher, Professor Wilfried Westheide, who made significant contributions to the reproductive biology of interstitial polychaetes, on the occasion of his 70th birthday.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Purschke, G., Jördens, J. Male genital organs in the eulittoral meiofaunal polychaete Stygocapitella subterranea (Annelida, Parergodrilidae): ultrastructure, functional and phylogenetic significance. Zoomorphology 126, 283–297 (2007). https://doi.org/10.1007/s00435-007-0047-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-007-0047-z

Keywords

Navigation