Skip to main content
Log in

New data on the ultrastructure of the proboscis in females of Bonellia viridis (Annelida: Bonellinae)

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

Abstract

Although Bonellia viridis is the best studied echiurid species, many features of its anatomy and ultrastructure are still unclear. Detailed data on the organisation of the proboscis may help us to understand the echiurid biology and some aspects of their feeding behaviour. In this study, a detailed description of the proboscis epithelium of females of B. viridis is provided. According to histological specificities, four zones of proboscis stem can be distinguished: dorsal, ventral, and two lateral. These zones differ from each other in ciliation and abundance of bonellin-producing and gland cells. Each zone provides certain functions: protective for dorsal, transport of food particles for ventral, and agglutination of food particles for lateral. Ciliated cells have been described in the epithelium of the dorsal side of the proboscis stem for the first time. These cells probably supply the slow ciliary movements of the proboscis. For the first time, the organisation of epithelial cells is described: these cells contain many pinocytotic vesicles, multivesicular bodies, and phagosomes, whose presence may provide evidence of the ability of epithelial cells to consume nutrients. The absence of continuous basal lamina under the ventral epithelium is ascertained and may be explained by the activity of bonellin-producing cells, which constantly penetrate between epithelial cells. In bonellin-producing cells, voluminous perinuclear space and the contribution of rough endoplasmic reticulum into the formation of bonellin-containing granules are detected for the first time. For the first time, the neurite bundles extending from lateral nerve cords to gland cells and bonellin-producing cells are discovered.

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

Similar content being viewed by others

References

  • Agius L, Jaccarini V (1981) Effects of light in pigment development in the echuran worm Bonellia viridis. J Zool 193:33–37

    Article  Google Scholar 

  • Amor A (1973) Modelos de sistema vascular en Echiura. Asoc Argent Ciencias Nat Physis Buenos Aires 32:115–120

    Google Scholar 

  • Baltzer F (1931) Echiurida. In: Kückenthal W, Krumbach T (eds) Handbuch Der Zoologie. DeGruyter, Berlin, pp 62–168

    Google Scholar 

  • Biseswar R (1991) Burrowing, locomotion and other movements of the Echiuran Ochetostoma caudex. Acta Zool 72:91–99. https://doi.org/10.1111/j.1463-6395.1991.tb00321.x

    Article  Google Scholar 

  • Bosch C (1977) Les cellules pigmentaires vertes de la Bonellie (Bonellia viridis Echmren) et leur role physiologique. C R Acad Sci (paris) 284:2123–2126

    Google Scholar 

  • Bosch C (1979) Ultrastructure et comportment des cellules pigmentaires vertes de Bonellia viridis (Echrnren). Ann Sci Nat Zool 1:223–249

    Google Scholar 

  • Bosch C (1981) La musculature, le squelette conjonctif et les mouvements de la trompe de la Bonellie (Bonellia viridis, Echiuridae). Ann Sci Nat Zool 3:203–229

    Google Scholar 

  • Bosch C (1984) Les vaisseaux sanguins de la trompe chez Bonellia viridis (Echmrien) et leur musculature a fonction multiple. Ann Sci Nat Zool 6:3–32

    Google Scholar 

  • Bosch C, Michel C (1979) Ultrastructural and histochemical study of the glands of the proboscis in Bonellia viridis Echiura. Cell Mol Biol 25:233–246

    CAS  Google Scholar 

  • Fisher WK, MacGinitie GE (1928) A new echiuroid worm from California. Ann Mag Nat Hist (series 10) 1:199–204

    Article  Google Scholar 

  • Goto R, Sakamoto S, Hayakawa J, Seike K (2016) Underwater observations of the giant spoon worm Ikeda taenioides (Annelida: Echiura: Ikedidae) in a subtidal soft-bottom environment in northeastern Japan, which survived tsunamis of the 2011 off the Pacific Coast of Tohoku Earthquake. J Oceanogr 73:103–113. https://doi.org/10.1007/s10872-016-0380-2

    Article  CAS  Google Scholar 

  • Goto R, Monnington J, Sciberras M, Hirabayashi I, Rouse GW (2020) Phylogeny of Echiura updated, with a revised taxonomy to reflect their placement in Annelida as sister group to Capitellidae. Invertebr Syst 34:101–111. https://doi.org/10.1071/IS19020

    Article  Google Scholar 

  • Hughes DJ, Crisp DJ (1976) A further description of the echiuran Prashadus pirotansis. J Zool 180:233–242

    Article  Google Scholar 

  • Hughes DJ, Ansell AD, Atkinson RJA, Nickell LA, Ansell AD, Atkinson RJA, Nickell LA (1993) Underwater television observations of surface activity of the echiuran worm Maxmuelleria lankesteri (Echiura: Bonelliidae). J Nat Hist 27:219–248. https://doi.org/10.1080/00222939300770081

    Article  Google Scholar 

  • Ikeda I (1904) The gephyrea of Japan. J Coll Sci Imp Univ Tokyo, Jpn 18:1–87

  • Jaccarini V, Schembri PJ (1977a) Feeding and particle selection in the echiuran worm Bonellia viridis Rolando (Echiura: Bonelliidae). J Exp Mar Bio Ecol 28:163–181

    Article  Google Scholar 

  • Jaccarini V, Schembri PJ (1977b) Locomotory and other movements of the proboscis of Bonellia viridis (Echiura, Bonellidae). J Zool Lond 182:467–476

    Article  Google Scholar 

  • Jaccarini V, Schembri PJ (1979) The proboscis ciliation of the echiuran Bonellia viridis. J Mar Biol Assoc UK 59:377–384

    Article  Google Scholar 

  • Jumars PA, Dorgan KM, Lindsay SM (2015) Diet of worms emended: an update of polychaete feeding guilds. Annu Rev Mar Sci 7:497–520. https://doi.org/10.1146/annurev-marine-010814-020007

    Article  Google Scholar 

  • Kawaguti S (1968) Electron microscopy on blue-green algae in the body-wall of an echiuro1d Jkedosoma gogoshimense. Biol Jpn Okayairna Univ 14:67–74

    Google Scholar 

  • Kharlamenko VI, Maiorova AS, Ermolenko EV (2018) Fatty acid composition as an indicator of the trophic position of abyssal megabenthic deposit feeders in the Kuril Basin of the Sea of Okhotsk. Deep Res Part II Top Stud Oceanogr. https://doi.org/10.1016/j.dsr2.2018.03.005

    Article  Google Scholar 

  • Kuznetsov PA, Maiorova AS, Temereva EN (2021) New data on echiuran anatomy and histology: the case of Lissomyema mellita (annelida: Thalassematidae). Zool. https://doi.org/10.1016/j.zool.2020.125865

    Article  Google Scholar 

  • Maiorova AS, Adrianov AV (2020) Biodiversity of echiurans (Echiura) of the Kuril-Kamchatka Trench area. Prog Oceanogr. https://doi.org/10.1016/j.pocean.2019.102216

    Article  Google Scholar 

  • Pilger JF (1977) Biology and Gametogenesis of Listriolobus pelodes (Echiura). Dissertation, University of Southern California

  • Pilger JF (1993) Echiura. In: Microscopic analomy of invertebrates, Volume 12: onychophora, chilopoda, and lessser protostomata. Willey-Liss Inc, pp 186–236.

  • Temereva EN, Kuznetsov PA, Kiseleva EA (2017) The morphology and microscopic anatomy of the deep-sea echiurid Protobonellia zenkevitchi Murina, 1976. Russ J Mar Biol 43:447–464. https://doi.org/10.1134/S1063074017060104

    Article  Google Scholar 

  • Vracko R (1974) Basal lamina scaffold. Anatomy and significance for maintenance of orderly tissue structure. Am J Path 77:314–346

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was conducted with financial support from the Russian Science Foundation (#18-04-00082-P), Russian Foundation for Basic Research (#20-04-00096), and supported by the Vernadski Grant of the French Embassy in the Russian Federation. The research was performed at the User Facilities Center of M.V. Lomonosov Moscow State University with financial support from the Ministry of Education and Science of the Russian Federation. The study was also supported by a Moscow State University Grant for Leading Scientific Schools "Depository of the Living Systems" within the MSU Development Program. The work of AE was conducted under the IDB RAS Government basic research program in 2021 № 0088-2021-0009. We thank the Morphology Service of the Mediterranean Institute of Marine and Terrestrial Biodiversity and Ecology (IMBE) for technical support. We are grateful to Laurent Vanbostal, OSU Pytheas, Marseille for Bonnelia viridis collection.

Author information

Authors and Affiliations

Authors

Contributions

PK performed the histology, prepared the serial sections, made some schemes, and photographed the sections. AE collected and fixed the animals, helped interpret the results, and helped to write the manuscript. ET prepared all figures, wrote the manuscript, and interpreted the results.

Corresponding author

Correspondence to Elena Temereva.

Ethics declarations

Conflict of interest statement

The authors declare that they do not have any conflict of interest. All authors have read the text and approved the final version of the manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kuznetsov, P., Ereskovsky, A. & Temereva, E. New data on the ultrastructure of the proboscis in females of Bonellia viridis (Annelida: Bonellinae). Zoomorphology 140, 453–468 (2021). https://doi.org/10.1007/s00435-021-00541-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-021-00541-5

Keywords

Navigation