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Innervation of Unpaired Branchial Appendages in the Annelids Terebellides cf. stroemii (Trichobranchidae) and Cossura pygodactylata (Cossuridae)

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Abstract—

We studied the innervation of unpaired branchial appendages using confocal laser scanning microscopy in two annelid species: Terebellides cf. stroemii (Trichobranchidae) and Cossura pygodactylata (Cossuridae). The branchial filament was found to be innervated by one unpaired segmental nerve coming from the ventral nerve cord at the level of chaetiger 2 in C. pygodactylata. This nerve lies transversally along the body wall and comes laterally to the base of the branchial filament. Such a structure indicates that (1) the branchial filament is unpaired and neither represents merged paired branchiae nor is related in its origin to prostomial appendages or peristomial ones, and (2) the branchial filament is the result of a shift of one of the paired segmental branchiae with parallel reduction of the second branchia in this pair. The branchial organ of T. cf. stroemii is innervated by paired segmental nerves from the first and second chaetigers. The segmental nerves are connected by longitudinal nerves going on the lateral sides of the body closer to the dorsum. One nerve on each side proceeds to the anterior part of the branchial stalk, and another nerve proceeds to the posterior part. All these nerves have transversal connections. The anterior stalk nerves come into the anterior branchial lobes, while the posterior nerves come to the posterior lobes. In the branchial lobes, the nerves give rise to thinner nerves, which go to each of the branchial lamellae. The present study confirms that the branchial organ of Terebellides has a paired nature and originates from segmental branchiae. Based on the number of innervating segmental nerves, we can conclude that the branchial organ of T. cf. stroemii is formed by two pairs of merged branchiae.

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REFERENCES

  1. Beklemishev, V.N., Osnovy sravnitel’noi anatomii bespozvonochnykh (Principles of Comparative Anatomy of Invertebrates), Moscow: Sovetskaya nauka, 1944.

  2. Fournier, J.A. and Petersen, M.E., Cossura longocirrata: redescription and distribution, with notes on reproductive biology and a comparison of described species of Cossura (Polychaeta: Cossuridae), Ophelia Suppl., 1991, vol. 5, pp. 63–80.

  3. Gustafson, G., Anatomische studien über die polychäten-familien amphinomidae und euphrosynidae, Zoologiska Bidrag fran Uppsala, 1930, vol. 12, pp. 305–482.

  4. Holthe, T., Evolution, systematics and distribution of the Polychaeta Terebellomorpha, with a catalogue of the taxa and a bibliography, Gunneria, Trondheim, 1986, vol. 55, pp. 1–236.

    Google Scholar 

  5. Holthe, T., Polychaeta Terebellomorpha, in Marine Invertebrates of Scandinavia, Trondheim: Norwegian University, 1986a, vol. 7.

    Google Scholar 

  6. Hutchings, P. and Peart, R., A revision of the Australian Tichobranchidae (Polychaeta), Invertebr. Syst., 2000, vol. 14, no. 2, pp. 225–272.

    Article  Google Scholar 

  7. Jouin-Toulmond, C. and Hourdez, S., Morphology, ultrastructure and functional anatomy of the branchial organ of Terebellides stroemii (Polychaeta: Trichobranchidae) and remarks on the systematic position of the genus Terebellides, Cahiers de biologie marine, 2006, vol. 47, no. 3, pp. 287–299.

    Google Scholar 

  8. Michel, C., Bhaud, M., Boumati, P., and Halpern, S., Physiology of the digestive tract of the sedentary polychaete Terebellides stroemi, Mar. Biol., 1984, vol. 83, no. 1, pp. 17–31.

    Article  Google Scholar 

  9. Muir, A.I., A redescription of Unobranchus (Annelida: Terebellida: Trichobranchidae), with notes on the systematics of Trichobranchidae, Ital. J. Zool., 2011, vol. 78, no. 1, pp. 140–147.

    Article  Google Scholar 

  10. Orrhage, L., On the anatomy of the central nervous system and the morphological value of the anterior end appendages of Ampharetidae, Pectinariidae and Terebellidae (Polychaeta), Acta Zool., 2001, vol. 82, no. 1, pp. 57–71.

    Article  Google Scholar 

  11. Orrhage, L. and Müller, M.C.M., Morphology of the nervous system of Polychaeta (Annelida), Hydrobiologia, 2005, vols. 535/536, pp. 79–111.

    Article  Google Scholar 

  12. Parapar, J., Moreira, J., and O’Reilly, M., A new species of Terebellides (Polychaeta: Trichobranchidae) from Scottish waters with an insight into branchial morphology, Mar. Biodivers., 2016, vol. 46, no. 1, pp. 211–225.

    Article  Google Scholar 

  13. Purschke, G., Sense organs and central nervous system in an enigmatic terrestrial polychaete, Hrabeiella periglandulata (Annelida): implications for annelid evolution, Invertebr. Biol., 2000, vol. 119, no. 3, pp. 329–341.

    Article  Google Scholar 

  14. Purschke, G., Hugenschütt, M., Ohlmeyer, L., Meyer, H., and Weihrauch, D., Structural analysis of the branchiae and dorsal cirri in Eurythoe complanata (Annelida, Amphinomida), Zoomorphology, 2016, vol. 1, no. 136, pp. 1–18.

    Google Scholar 

  15. Remane, A., Über die Homologisierungsmöglichkeiten bei Verbindungsstrukturen (Muskeln, Blutgefäßen, Nerven) und Hohlräumen, Zoologischer Anzeiger, 1963, vol. 170, pp. 481–489.

    Google Scholar 

  16. Rimskaya-Korsakova, N.N., Kristof, A., Malakhov, V.V., and Wanninger, A., Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida), Front. Zool., 2016, vol. 13, no. 1, pp. 1–18.

    Article  CAS  Google Scholar 

  17. Rouse, G. and Pleijel, F., Polychaetes, Oxford: Oxford Univ. Press, 2001.

    Google Scholar 

  18. Rouse, G.W. and Tzetlin, A.B., Ultrastructure of the body wall and gametogenesis in Cossura cf. longocirrata (Cossuridae Polychaeta), Invertebr. Reprod. Dev., 1997, vol. 32, no. 1, pp. 41–54.

    Article  Google Scholar 

  19. Steen, J., Anatomisch-histologische untersuchung von Terebellides stroemii M. Sars, Jenaische Zeitschrift für Naturwissenschaft, 1883, vol. 16, pp. 201–246.

    Google Scholar 

  20. Storch, V. and Alberti, G., Ultrastructural observations on the gills of polychaetes, Helgoländer Wissenschaftliche Meeresuntersuchungen, 1978, vol. 31, no. 1, pp. 169–179.

    Article  Google Scholar 

  21. Tzetlin, A.B., Fine morphology of the feeding apparatus of Cossura sp. (Polychaeta, Cossuridae) from the White Sea, Memoires du Museum national D’histoire naturelle, 1994, vol. 162, pp. 137–143.

  22. Tzetlin, A. and Zhadan, A., Morphological variation of axial non-muscular proboscis types in the Polychaeta, Zoosymposia, 2009, vol. 2, no. 1, pp. 415–427.

    Google Scholar 

  23. Ushakov, P.V., Mnogoshchetinkovye chervi dal’nevostochnykh morei SSSR (Polychaeta) (Polychaetes of the Far Eastern Seas of the USSR (Polychaeta)), Moscow: Akad. Nauk SSSR, 1955.

  24. Zhadan, A.E., Vortsepneva, E.V., and Tzetlin, A.B., Redescription and biology of Cossura pygodactylata Jones, 1956 (Polychaeta: Cossuridae) in the White Sea, Invertebr. Zool., 2012, vol. 9, no. 2, pp. 115–125.

    Article  Google Scholar 

  25. Zhadan, A.E., Vortsepneva, E.V., and Tzetlin, A.B., Three-dimensional reconstruction of the musculature of Cossura pygodactylata Jones, 1956 (Annelida: Cossuridae), Zoologischer Anzeiger—J. Comp. Zool., 2014, vol. 253, no. 3, pp. 181–191.

    Google Scholar 

  26. Zhadan, A.E., Vortsepneva, E.V., and Tzetlin, A.B., Ontogenetic development and functioning of the anterior end of Cossura pygodactylata Jones, 1956 (Annelida: Cossuridae), Zoomorphology, 2015, vol. 134, no. 4, pp. 509–521.

    Article  Google Scholar 

  27. Zhirkov, I.A., Polikhety Severnogo ledovitogo okeana (Polychaetes of the Arctic Ocean), Moscow: Yanus-K, 2001.

    Google Scholar 

  28. Zrzavý, J., Říha, P., Piálek, L., and Janouškovec, J., Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes, BMC Evol. Biol., 2009, vol. 9, no. 1, p. 189. doi 10.1186/1471-2148-9-189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

The authors are grateful to N.N. Rimskaya-Korsakova for a helpful review.

This study (material collection of section preparation) was supported by the Russian Foundation for Basic Research, project nos. 15-04-05875, 15-29-02447, and 16-04-00343. The part of the study conducted using the confocal laser scanning microscope was supported by the Russian Science Foundation, project no. 14-50-00029.

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  1. Department of Biology, Moscow State University, 119234, Moscow, Russia

    A. B. Tzetlin, A. E. Zhadan & E. V. Vortsepneva

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  1. A. B. Tzetlin
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  2. A. E. Zhadan
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  3. E. V. Vortsepneva
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Correspondence to A. B. Tzetlin.

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Translated by Ya. Lavrenchuk

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Tzetlin, A.B., Zhadan, A.E. & Vortsepneva, E.V. Innervation of Unpaired Branchial Appendages in the Annelids Terebellides cf. stroemii (Trichobranchidae) and Cossura pygodactylata (Cossuridae). Biol Bull Russ Acad Sci 45, 659–668 (2018). https://doi.org/10.1134/S1062359018070166

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