Structure of Male Reproductive System in Spirula (Cephalopoda: Spirula spirula)

R.M. Sabirov*, A.A. Novikov**, A.V. Golikov***

Kazan Federal University, Kazan, 420008 Russia

E-mail: *Rushan.Sabirov@mail.ru, **aan201097@yandex.ru, ***Golikov_ksu@mail.ru

Received June 15, 2017

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Abstract

This paper provides a des­cription of general morphology of the reproductive system in male specimens of Spirula spirula, including morphometric characters of spermatophores and features of their production during the ontogenesis. The reproductive system fitted the general scheme of Coleoidea. However, the position of the reproductive system in the body of the studied male specimens was uncommon for all known Cephalopoda: the testis and spermatophoric complex (SC) were located posteriorly into the mantle cavity to the right and to the left from the middle body line, respectively. This symmetric lateral location can be attributed to the development of the internal spiral shell. To connect the testis and SC, an extremely elongated coelomoduct (reproductive funnel) developed. It runs through the empty cavity inside the first (internal) whorl of the shell. Spermatophores were morphologically characterized by the distinguishing structure of their cement body. Spermatophore length was 10.81–12.07 mm, mean length was 11.37 mm, which was 29.2% of mantle length (ML). The quantity of sperm packed in the seminal reservoirs of spermatophores continuously decreased during the ontogenesis. Spermatophore number in the spermatophoric sac was 84, total volume of sperm packed in all spermatophores was 0.0168 cm3, mean mass of the spermatophore was 0.65 mg, total mass of all spermatophores in the spermatophoric sac was 0.021 g. In general, the reproductive system in male specimens of Spirula bears the signs of high specialization (unique topography, elongated coelomoduct, continuous decreasing spermatophorogenesis), which developed during the evolution of ratio of their endogastric shell and visceral inner sac.

Keywords: Spirula, male reproductive system, functional morphology, spermatophores, ontogenetic variability


Figure Captions

Fig. 1. The reproductive system in male specimens of Spirula: a – position of the testis and spermatophoric complex (SC) in the mantle cavity, ventral view; b – SC, ventral view; c – SC, flattened view; d – testis, view from the medial side adjacent to the shell; e – a photo of the testis fragment with the radial position of seminiferous tubules. Scale: a, d – 1 cm; b, c – 0.5 mm; e – 0.1 mm. 1 – shell; 2 – testis; 3 – coelomoduct (reproductive funnel); 4 – spermiduct; 5–10 – regions I–VI of the spermatophoric gland, respectively; 11 – spermatophoric (Needham's sac) sac; 12 – penis.

Fig. 2. The spermatophore of Spirula: a – external view; b – bulb; c – cement body with the adjacent region of the ejaculatory tube; d – the region of connection between the cement body and the seminal reservoir; e – posterior hollow part of the spermatophore. Scale: a – 1 cm; b, c, d – 5 mm; d – 2 mm.

References

  1. Nesis K.N. Abridged Manual to the Cephalopods of the World's Ocean. Moscow, Legk. Pishch. Prom-st., 1982. 360 p. (In Russian)
  2. Schmidt J. Live specimens of Spirula. Nature, 1922, vol. 110, no. 2771, pp. 788–790.
  3. Mercer M.C. A synopsis of recent cephalopoda of Canada. Part 2. Fish. Res. Board Can. Stud., 1969, no. 1327, pp. 55–65.
  4. Jereb P., Roper C.F.E. Cephalopods of the World. An Annotated and Illustrated Catalogue. Vol. 1. Chambered Nautiluses and Sepioids. Rome, 2005. 262 p.
  5. Bruun A.F. The biology of Spirula spirula (L.). Dana Rep., Carlsberg Found., 1943, vol. 24, pp. 1–46.
  6. Haring E., Kruckenhauser L., Lukeneder A. New DNA sequence data on the enigmatic Spirula spirula (Linnaeus, 1758) (Decabrachia, suborder Spirulina). Ann. Naturhist. Mus. Wien, Ser. B, 2012, vol. 113, pp. 37–48.
  7. Bizikov V.A. Evolution of the Shell in Cephalopoda. Moscow, VNIRO, 2008. 448 p. (In Russian)
  8. Owen R. On the external and structural characters of the male Spirula australis, Lam. Proc. Zool. Soc. London, 1880, pp. 352–354.
  9. Chun C. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition auf dem Dampfer “Valdivia” 1898–1899. Die Cephalopoden. II. Teil: Myopsida, Octopoda. Chun C., Brauer A. (Eds.). Jena, Gustav Fischer, 1915, vol. 18. pp. 405–552.
  10. Naef A. Die Cephalopoden. Fauna und Flora des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Monographie 35. Berlin, Verlag von R. Friedlander & Sohn, 1921–1923, T. I, Bd. 1–2, pp. 1–863.
  11.  Kerr J.G. Notes upon the Dana specimens of Spirula and upon certain problems of Cepholopod morphology. The Danish “Dana”-Expeditions 1920–22 in the North Atlantic and the Gulf of Panama: Oceanographical reports edited by the “Dana” Committee, 1931, no. 8, pp. 1–35.
  12. Clarke M.R. Growth and development of Spirula spirula. J. Mar. Biol. Assoc., 1970, vol. 50, pp. 53–64. doi: 10.1017/S002531540000059X.
  13. Nigmatullin Ch.M., Sabirov R.M., Zalygalin V.P. Ontogenetic aspects of morphology, size, structure and production of spermatophores in ommastrephid squids: An overview. Berl. Palabiol. Abh., 2003, Bd. 3, pp. 80–96.
  14. Sabirov R.M. Reproductive system in males of Cephalopoda. II. Spermatophoric complex of organs. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2009, vol. 151, no. 2, pp. 34–51. (In Russian)
  15. Sabirov R.M. Reproductive system in males of Cephalopoda. III. Spermatophores. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2010, vol. 152, no. 2, pp. 8–21. (In Russian)
  16. Golikov A.V., Sabirov R.M. The reproductive system morphology and reproductive strategies of bobtail squids in the Arctic (Cephalopoda: Sepiolida). Abstr. Int. Congr. on Invertebrate Morphology ICIM-4, August 18–23, 2017, Moscow. Moscow, Pero, 2017, p. 217.
  17. Healy J.M. Ultrastructure of spermatozoa and spermiogenesis in Spirula spirula (L.): Systematic importance and comparison with other cephalopods. Helgoländer Meeresunters., 1990, vol. 44, pp. 109–123. doi: 10.1007/BF02365434.
  18. Warnke K., Plotner J., Santana J.I., Rueda M.J., Llinas O. Reflections on the phylogenetic position of Spirula (Cephalopoda): Preliminary evidence from the 18S ribosomal RNA gene. Berl. Paläobiol. Abh., 2003, Bd. 3, S. 253–260.
  19. Lindgren A.R., Pankey M.S., Hochberg F.G., Oakley T.H. A multi-gene phylogeny of Cephalopoda supports convergent morphological evolution in association with multiple habitat shifts in the marine environment. BMC Evol. Biol., 2012, vol. 12, art. 129, pp. 1–15. doi: 10.1186/1471-2148-12-129.
  20. Strugnell J.M., Hall N.E., Vecchione M., Fuchs D., Allcock A.L. Whole mitochondrial genome of theRam's Horn Squid shines light on the phylogenetic position of the monotypic order Spirulida (Haeckel, 1896). Mol. Phylogenet. Evol., 2017, vol. 109, pp. 296–301. doi: 10.1016/j.ympev.2017.01.011.
  21. Warnke K., Keupp H. Spirula – a window to the embryonic development of ammonoids? Morphological and molecular indications for a palaeontological hypothesis. Facies, 2005, vol. 51, nos. 1–4, pp. 60–65. doi: 10.1007/s10347-005-0054-9.
  22. Mutvei H., Donovan D.T. Siphuncular structure in some fossil coleoids and recent Spirula. Paleontology, 2006, vol. 49, no. 3, pp. 685–691. doi: 10.1111/j.1475-4983.2006.00533.x.
  23. Hoffman R., Warnke K. Spirula – das unbekannte Wesen aus der Tiefsee. Denisia 32, zugleich Kataloge des oberösterreichischen Landesmuseums Neue Serie, 2014, Bd. 157, S. 33–46. (In German)


For citation: Sabirov R.M., Novikov A.A., Golikov A.V. Structure of male reproductive system in Spirula (Cephalopoda: Spirula spirula). Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2017, vol. 159, no. 3, pp. 433–442. (In Russian)


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