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Zoomorphology

, Volume 131, Issue 2, pp 171–184 | Cite as

A place for nourishment or a slaughterhouse? Elucidating the role of spermathecae in the terrestrial annelid Hormogaster elisae (Clitellata: Opisthopora: Hormogastridae)

  • Marta Novo
  • Ana Riesgo
  • Carmen Roldán
  • Gonzalo Giribet
  • Darío J. Díaz Cosín
Original Paper

Abstract

The capacity of storing sperm within the female reproductive tract occurs widely across vertebrate and invertebrate species. Although the type and position of spermathecae have been commonly used as a taxonomic character in Opisthopora, few studies have focused on the ultrastructural description of these interesting storage organs. This study is the first to report on the ultrastructure of the spermathecae and spermatozoa of Hormogaster elisae, an endemism of the central area of the Iberian Peninsula that presents two pairs of tubular spermathecae. Light and electron microscopy showed that the spermathecae are full of highly packed spermatozoa embedded in an electron-dense substance. Two layers constitute the spermathecal wall. The outer layer consists of peritoneal cells, collagenous basal laminae at different levels, several layers of striated muscle, and numerous blood vessels. The inner layer is a monostratified epithelium of prismatic cells presenting long and abundant microvilli probably for the maintenance of a favorable environment for the spermatozoa. The epithelial cells show high activity, and three different types of secretions were detected: holocrine, merocrine, and apocrine, whose hypothetical function on nourishment and/or causing quiescence is discussed here. Although no phagocytotic processes were detected, some sperm cells were observed in digestive vesicles within the cytoplasm of the epithelial cells, and there was also evidence of active sperm entrance into the epithelium. A place for nourishment or a slaughterhouse? Probably both.

Keywords

Annelida Opisthopora Spermathecae Spermatozoa Sperm digestion Transmission electron microscopy Secretions 

Notes

Acknowledgments

We are indebted to Rosa Fernández for field assistance and advice on sample preparation. We also thank Carolyn Marks and Adam Graham for their constant availability and help on sample processing and TEM imaging in the Center for Nanoscale Systems (CNS) at Harvard University. M.N. was supported by a Grant from Fundación Caja Madrid and A.R. by a Marie Curie Outgoing Fellowship. This research was funded by internal MCZ funds to G.G. and CGL2010/16032 from the Spanish Ministry of Science and Innovation to D.J.D.C. and C.R.

References

  1. Beese K, Armbruster GFJ, Beier K, Baur B (2009) Evolution of female sperm-storage organs in the carrefour of stylommatophoran gastropods. J Zool Syst Evol Res 47:49–60CrossRefGoogle Scholar
  2. Birkhead TR, Møller AP (1993) Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biol J Linn Soc 50:295–311CrossRefGoogle Scholar
  3. Birkhead TR, Møller AP, Sutherland WJ (1993) Why do females make it so difficult for males to fertilize their eggs? J Theor Biol 161:51–60CrossRefGoogle Scholar
  4. Bojat NC, Sauder U, Haase M (2001) The spermathecal epithelium, sperm and their interactions in the hermaphroditic land snail Arianta arbustorum (Pulmonata, Stylommatophora). Zoomorphology 120:147–157CrossRefGoogle Scholar
  5. Brinkhurst RO, Jamieson BGM (1971). Aquatic oligochaeta of the world. Oliver and Boyd, EdinburghGoogle Scholar
  6. Butt KR, Nuutinen V (1998) Reproduction of the earthworm Lumbricus terrestris Linné after the first mating. Can J Zool 76:104–109Google Scholar
  7. Dent JN (1970) The ultrastructure of the spermatheca in the red spotted newt. J Morphol 132:397–424PubMedCrossRefGoogle Scholar
  8. Díaz Cosín DJ, Ruiz MP, Ramajo M, Gutiérrez M (2006) Is the aestivation of the earthworm Hormogaster elisae a paradiapause? Inv Biol 125:250–255CrossRefGoogle Scholar
  9. Díaz Cosín DJ, Hernández P, Trigo D, Fernández R, Novo M (2009) Algunos aspectos del ciclo biológico del endemismo ibérico, Hormogaster elisae Álvarez, 1977 (Oligochaeta, Hormogastridae), en cultivos de laboratorio. Bol R Soc Esp Hist Nat Biol 103:49–57Google Scholar
  10. Díaz Cosín J, Novo M, Fernández R (2011) Reproduction of earthworms: sexual selection and parthenogenesis. In: Karaka A (ed) Biology of earthworms. Springer, Berlin, pp 69–86CrossRefGoogle Scholar
  11. Dixon G (1915) Tubifex. In: Herdman WA (ed) LMBC memoirs on typical British marine plants and animals, vol 23. Williams and Norgate, London, pp 1–100Google Scholar
  12. Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, CambridgeGoogle Scholar
  13. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, NJGoogle Scholar
  14. Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms, 3rd edn. Chapman and Hall, LondonGoogle Scholar
  15. Eisen G (1874) New Englands och Canadas Lumbricides. Ofversigt af Kongliga Vetenskaps-Akademiens Forhandligar Stockholm 31(2):41–49Google Scholar
  16. Fernández R, Bergmann P, Almodóvar A, Díaz Cosín DJ, Heethoff M (2011) Ultrastructural and molecular insights into three populations of Aporrectodea trapezoides (Dugés, 1828) (Oligochaeta, Lumbricidae) with different reproductive modes. Pedobiologia 54:281–290CrossRefGoogle Scholar
  17. Ferraguti M, Jamieson BGM (1984) Spermiogeness and spermatozoal ultrastructure in Hormogaster (Hormogastridae, Oligochaeta, Annelida). J Submicrosc cytol 16:307–316Google Scholar
  18. Fleming TP (1981) The ultrastructure of the spermathecae of Tubifex tubifex (Annelida: Oligochaeta). J Zool Lond 193:129–145CrossRefGoogle Scholar
  19. Garvín MH, Trigo D, Hernández P, Díaz Cosín DJ (2003) Gametogenesis and reproduction in Hormogaster elisae (Oligochaeta, Hormogastridae). Inv Biol 122:152–157CrossRefGoogle Scholar
  20. Grove AJ (1925) On the reproductive processes of the earthworm, Lumbricus terrestris. Q J Microsc Sci 69:245–290Google Scholar
  21. Grube E (1879) Zoology of Rodriguez. Annelida. Phil Trans R Soc London 168:554–556Google Scholar
  22. Gutiérrez M, Jesús JB, Trigo D, Díaz Cosín DJ (2006) Is Hormogaster elisae (Oligochaeta, Hormogastridae) a predator of mite and springtails? Eur J Soil Biol 42:S186–S190CrossRefGoogle Scholar
  23. Hellriegel B, Bernasconi G (2000) Female-mediated differential sperm storage in a fly with complex spermathecae, Scatophaga stercoraria. Anim Behav 59:311–317PubMedCrossRefGoogle Scholar
  24. Hilario A, Young CM, Tyler PA (2005) Sperm storage, internal fertilization, and embryonic dispersal in vent and seep tubeworms (Polychaeta: Siboglinidae: Vestimentifera). Biol Bull 208:20–28PubMedCrossRefGoogle Scholar
  25. Holt WV, Lloyd RE (2010) Sperm storage in the vertebrate female reproductive tract: how does it work so well? Theriogenology 73:713–722PubMedCrossRefGoogle Scholar
  26. Jamieson BGM (1981) The ultrastructure of the oligochaeta. Academic Press, London, p 462Google Scholar
  27. Jamieson BGM (1992) Oligochaeta. In: Harrison FW, Gardiner SL (eds) Microscopic anatomy of invertebrates, vol 7. Wiley-Liss, New YorkGoogle Scholar
  28. Jamieson BGM (2001) Native earthworms of Australia (Megascolecidae, Megascolecinae). Science Publishers, Inc., EnfieldGoogle Scholar
  29. Jamieson BGM (2006) Non-leech Clitellata. In: Reproductive biology and phylogeny of annelida. Series Editor Jamieson BGM. Rouse G, Pleijel F (eds), vol 4. Chap. 8. Science Publishers, EnfieldGoogle Scholar
  30. Linnæus C (1758) Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. pp [1–4], 1–824. Holmiæ. (Salvius)Google Scholar
  31. McCoy F (1878) Megascolides australis (McCoy). The giant earth-worm. Prodromus Zool Vic 1:21–25Google Scholar
  32. Meyer WJ, Bowman H (1994) Mating period and cocoon production in Eisenia fetida. The 5th international symposium on earthworm ecology Columbus Ohio, 5–9, p 128Google Scholar
  33. Novo M, Almodóvar A, Díaz Cosín DJ (2009) High genetic divergence of hormogastrid earthworms (Annelida, Oligochaeta) in the central Iberian Peninsula: evolutionary and demographic implications. Zool Scripta 38:537–552CrossRefGoogle Scholar
  34. Novo M, Almodóvar A, Fernández R, Trigo D, Díaz Cosín DJ (2010a) Cryptic speciation of hormogastrid earthworms revealed by mitochondrial and nuclear data. Mol Phylogenet Evol 56:507–512PubMedCrossRefGoogle Scholar
  35. Novo M, Almodóvar A, Fernández R, Gutiérrez M, Díaz Cosín DJ (2010b) Mate choice of an endogeic earthworm revealed by microsatellite markers. Pedobiologia 53:375–379CrossRefGoogle Scholar
  36. Novo M, Almodóvar A, Fernández R, Giribet G, Díaz Cosín DJ (2011) Understanding the biogeography of a group of earthworms in the Mediterranean basin—the phylogenetic puzzle of Hormogastridae (Clitellata: Oligochaeta). Mol Phylogenet Evol 61:125–135PubMedCrossRefGoogle Scholar
  37. Qiu JP, Bouché MB (1998) Contribution to the taxonomy of Hormogastridae (Annelida: Oligochaeta) with description of new species from Spain. Doc Pedozool Integrol 4:164–177Google Scholar
  38. Rafinesque CS (1820) Ichthyologia Ohiensis. Reprinted edition: Burrows Brothers Co., Cleveland, 1899Google Scholar
  39. Richards KS, Fleming TP (1982) Spermatozoal phagocytosis by the spermathecae of Dendrobaena subrubicunda and other lumbricids (Oligochaeta, Annelida). Int J Invert Rep 5:233–241Google Scholar
  40. Rosa D (1887) Hormogaster redii n. g., n. sp. Bollettino dei Musei di Zoologia ed Anatomia comparata della Universita di Torino 32(II)Google Scholar
  41. Savigny JC (1826) In Cuvier, Analyse des travaux de l’Academie Royale des Sciences pendant l’année 1821, partie physique. Mem Acad Roy Sci Inst Fr 5:176–184Google Scholar
  42. Teisaire ES, Roldán IA (1995) Ultrastructure and histochemistry of the spermatheca of Amynthas Kinberg and Metaphire Sims and Easton (Oligochaeta: Megascolecidae). Comun Biol 13:169–181Google Scholar
  43. Valle JV, Moro RP, Garvín MH, Trigo D, Díaz Cosín DJ (1997) Annual dynamics of the earthworm Hormogaster elisae (Oligochaeta, Hormogastridae) in Central Spain. Soil Biol Biochem 29:309–312CrossRefGoogle Scholar
  44. Vanpraagh BD (1995) Reproductive biology of Megascolides australis McCoy (Oligochaeta: Megascolecidae). Aust J Zool 43:489–507CrossRefGoogle Scholar
  45. Varuta AT, More NK (1972) Cytochemical study of mucus and mucus secreting cells in spermathecae of the earthworms, Pheretima elongata (Perrier) and Hoplochaetella powelli (Michaelsen). Ind Exp Biol 10:239–241Google Scholar
  46. Vyas I, Dev B (1972) Histochemical localization of alkaline phosphatase in the spermathecae of the earthworm, Barogaster annandalei (Stephenson). Acta Histochem 42:344–350PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Marta Novo
    • 1
    • 2
  • Ana Riesgo
    • 1
  • Carmen Roldán
    • 2
  • Gonzalo Giribet
    • 1
  • Darío J. Díaz Cosín
    • 2
  1. 1.Department of Organismic and Evolutionary Biology, Museum of Comparative ZoologyHarvard UniversityCambridgeUSA
  2. 2.Departamento de Zoología y Antropología Física, Facultad de BiologíaUniversidad Complutense de MadridMadridSpain

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