Reproductive cycle of Antedon mediterranea (Crinoidea, Echinodermata): correlation between morphology and physiology

Abstract

Gonads of the mediterranean crinoid Antedon mediterranea were analyzed in order to reconstruct their histological organization. The tissue arrangement resembled that previously described in other crinoids. Five reproductive stages were identified in both males and females: recovery, growing, premature, mature, spent. Sexually dimorphic characters were observed at the gonopore level. Hermaphroditic individuals were never detected. There were novel findings concerning somatic accessory cells of the gonads. The reproductive cycle periodicity was indicated by analysis of reproductive stage frequencies in the period 2003–2005: spring and winter were the seasons with highest and lowest maturity levels, respectively. A role in the regulation of reproduction was hypothesized for testosterone and 17β-estradiol, which were found to be present in A. mediterranea tissues and to vary during the reproductive cycle, thus suggesting a correlation between steroid levels and morphologically recognizable reproductive stages.

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References

  1. Barbaglio A, Mozzi D, Sugni M, Tremolada P, Bonasoro F, Lavado R, Porte C, Candia Carnevali MD (2006) Effects of exposure to ED contaminants (TPT-Cl and Fenarimol) on crinoid echinoderms: comparative analysis of regenerative development and correlated steroid levels. Mar Biol (Berl) 149:65–77. doi:10.1007/s00227-005-0205-0

    Article  CAS  Google Scholar 

  2. Barbaglio A, Sugni M, Di Benedetto C, Bonasoro F, Schnell S, Lavado R, Porte C, Candia Carnevali MD (2007) Gametogenesis correlated with steroid levels during the gonadal cycle of the sea-urchin Paracentrotus lividus (Echinodermata: Echinoidea). Comp Biochem Physiol A 147:466–474

    Google Scholar 

  3. Bickell L, Chia FS, Crawford BJ (1980) A fine structural study of the testicular wall and spermatogenesis in the crinoid Florometra serratissima (Echinodermata). J Morphol 166:109–126. doi:10.1002/jmor.1051660108

    Article  Google Scholar 

  4. Candia Carnevali MD (2005) Regenerative response and endocrine disrupters in Crinoid Echinoderms: an old experimental model, a new ecotoxicological test. In: Matranga V (ed) Progress in molecular and subcellular biology subseries marine molecular biotechnology. Echinodermata. Springer, Heidelberg, pp 167–199

    Google Scholar 

  5. Candia Carnevali MD, Bonasoro F (2001) Microscopic overview of crinoid regeneration. Microsc Res Tech 55:403–426. doi:10.1002/jemt.1187

    PubMed  Article  CAS  Google Scholar 

  6. Candia Carnevali MD, Bonasoro F, Patruno M, Thorndyke MC, Galassi S (2001) PCB exposure and regeneration in crinoids (Echinodermata). Mar Ecol Prog Ser 215:155–167. doi:10.3354/meps215155

    Article  Google Scholar 

  7. Chia FS, Atwood D, Crawford B (1975) Comparative morphology of Echinoderm sperm and possible phylogenetic implications. Am Zool 15:553–565

    Google Scholar 

  8. Clark AH (1921) A monograph of the existing crinoids. Bull US Natl Mus 82(1):1–795

    Google Scholar 

  9. Dan K, Kubota H (1960) Data on the spawning of Comanthus japonica between 1937 and 1955. Embryologia (Nagoya) 5(1):21–37. doi:10.1111/j.1440-169X.1960.tb00264.x

    Article  Google Scholar 

  10. Den Besten PJ (1998) Cytocrome P450 monoxygenase system in echinoderms. Comp Biochem Physiol 121(C):139–146

    Google Scholar 

  11. Dieleman SJ, Schoenmakers HJN (1979) Radioimmunoassay to determine the presence of progesterone and estrone in the starfish Asterias rubens. Gen Comp Endocrinol 39:534–542. doi:10.1016/0016-6480(79)90242-9

    PubMed  Article  CAS  Google Scholar 

  12. Dimelow EJ (1958). Some aspects of the biology of Antedon bifida (Pennant) with some reference to Neocomatella europa. PhD dissertation, University of Reading (UK)

  13. Fell HB (1966) Ecology of crinoids. In: Boolootian RA (ed) Physiology of Echinodermata. Wiley (Interscience), New York, pp 49–62

    Google Scholar 

  14. Haesaerts D, Jangoux M, Flammang P (2005) The attachment complex of brachilaria larvae of the sea star Asterias rubens (Echinodermata): an ultrastructural and immunocytochemical study. Zoomorphology 124:67–78. doi:10.1007/s00435-005-0112-4

    Article  Google Scholar 

  15. Harvey LA (1931) Studies on echinoderm oogenesis I. Antedon bifida. Proc R Soc Lond B Biol Sci 107:417–441

    Article  Google Scholar 

  16. Heinzeller T, Welsch U (1994) Crinoidea. In: Herrison F (ed) Microscopic anatomy of invertebrates: Echinodermata, vol 14. Wiley-Liss press, New York, pp 9–148

    Google Scholar 

  17. Hines GA, Watts SA, Sower SA, Walker CW (1992) Sex steroid levels in the testes, ovaries and pyloric caeca during gametogenesis in the sea star Asterias vulgaris. Gen Comp Endocrinol 87:451–460. doi:10.1016/0016-6480(92)90053-M

    PubMed  Article  CAS  Google Scholar 

  18. Holland ND (1988) Fine structure of oocyte maturation in a crinoid echinoderm, Oxycomanthus japonicus: a time-laps study by serial biopsy. J Morphol 198:205–217. doi:10.1002/jmor.1051980207

    Article  Google Scholar 

  19. Holland ND (1991) Echinodermata: Crinoidea. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates, vol 6. Boxwood, London, pp 247–299

    Google Scholar 

  20. Holland ND, Grimmer JC (1975) Epidermal mucus and the reproduction of a crinoid echinoderm. Nature 255:223–224. doi:10.1038/255223a0

    PubMed  Article  CAS  Google Scholar 

  21. Holland ND, Kubota H (1975) Fluctuations in the volume of non-geminal cell population during the annual reproductive cycle of Comanthus japonica (Echinodermata: Crinoidea). Annot Zool Jpn 48:83–89

    Google Scholar 

  22. Holland ND, Grimmer JC, Kubota H (1975) Gonadal development during the annual reproductive cycle of Comanthus japonica (Echinodermata: Crinoidea). Biol Bull 148:219–242. doi:10.2307/1540544

    PubMed  Article  CAS  Google Scholar 

  23. Hyman LH (1955) The invertebrates: Echinodermata, vol IV. Mc Graw-Hill, London, pp 34–119

    Google Scholar 

  24. Janer G, LeBlanc GA, Porte C (2005) A comparative study on the metabolism of androgens in invertebrates and its modulation by xenoandrogens. Gen Comp Endocrinol 143:211–221. doi:10.1016/j.ygcen.2005.03.016

    PubMed  Article  CAS  Google Scholar 

  25. Lavado R, Barbaglio A, Candia Carnevali MD, Porte C (2006a) Steroid levels in crinoid echinoderms are altered by exposure to endocrine disruptors. Steroids 71:489–497. doi:10.1016/j.steroids.2006.01.009

    PubMed  Article  CAS  Google Scholar 

  26. Lavado R, Sugni M, Candia Carnevali MD, Porte C (2006b) Triphenyltin alters androgen metabolism in the sea urchin Paracentrotus lividus. Aquat Toxicol 79:247–256. doi:10.1016/j.aquatox.2006.06.012

    PubMed  Article  CAS  Google Scholar 

  27. Lutz I, Sugni M, Candia Carnevali MD, Schulte-Oehlmann U, Kloas W (2006) Evidence for the existence of functioning sex steroid receptors in invertebrates: I. Specific androgen and estrogen binding sites in the echinoderms Paracentrotus lividus and Antedon mediterranea. Comp Biochem Physiol (submitted)

  28. McClintock JB, Pearse JS (1987) Reproductive biology of the common antarctic crinoid Promachocrinus kerguelensis (Echinodermata: Crinoidea). Mar Biol (Berl) 96:375–383. doi:10.1007/BF00412521

    Article  Google Scholar 

  29. Mita M (2000) 1-Methyladenine: a starfish oocyte maturation-inducing substance. Zygote 8(Suppl 1):9–11

    Google Scholar 

  30. Mladenov PV (1986) Reproductive biology of the feather star Florometra serratissima: gonadal structure, breeding pattern and the periodicity of ovulation. Can J Zool 64:1642–1651. doi:10.1139/z86-247

    Article  Google Scholar 

  31. Morcillo Y, Albalat A, Porte C (1999) Mussels as sentinels of organotin pollution: bioaccumulation and effects on P450-mediated aromatase activity. Environ Toxicol Chem 18:1203–1208

    Article  CAS  Google Scholar 

  32. Nichols D (1994) Reproductive seasonality in the comatulid crinoid Antedon bifida (Pennant) from the English Channel. Philos Trans R Soc Lond B 343:113–134. doi:10.1098/rstb.1994.0015

    Article  Google Scholar 

  33. Pearse JS, Cameron RA (1991) Echinodermata: Echinoidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates, echinoderms and lophophorates, vol VI. Boxwood Press, Pacific Grove, pp 514–664

    Google Scholar 

  34. Reichensperger A (1908) Über das Vorkommen von Drüsen bei Crinoiden. Zool Anz 33:363–367

    Google Scholar 

  35. Rutman JL (1975) The reproductive activity of the feather star Laprometra kluzingeri (Hartlaub) and Heterometra savignii (J. Müller) from the gulf of Elat (Red Sea). PhD dissertation, University of Tel-Aviv, Tel-Aviv, Israel

  36. Rutman JL, Fishelson L (1985) Comparison of reproduction in the Red Sea feather-stars Lamprometra kluzingeri (Hartlaub), Heterometra savignii (J. Müller) and Capillaster multiradiatus (L.). In: Keegan BF, O’Connor BDS (eds) Echinodermata: Proceedings of the 5th International Echinodermata Conference, Galway, Balkema, Rotterdam, pp 195–201

  37. Schoenmakers HJN, Dieleman SJ (1981) Progesterone and estrone levels in the ovaries, pyloric ceca and perivisceral fluid during the annual reproductive cycle of starfish Asterias rubens. Gen Comp Endocrinol 43:63–70. doi:10.1016/0016-6480(81)90032-0

    PubMed  Article  CAS  Google Scholar 

  38. Spirlet C, Grosjean P, Jangoux M (1998) Reproductive cycle of the echinoid Paracentrotus lividus: analysis by means of the maturity index. Invertebr Reprod Dev 34(1):69–81

    Google Scholar 

  39. Sugni M, Mozzi D, Barbaglio A, Bonasoro F, Candia Carnevali MD (2007) Endocrine disrupting compounds and echinoderms: new ecotoxicological sentinels for the marine ecosystem. Ecotoxicology 16(1):95–108. doi:10.1007/s10646-006-0119-8

    PubMed  Article  CAS  Google Scholar 

  40. Sugni M, Barbaglio A, Tremolada P, Candia Carnevali MD (2008). New tools and strategies for biomonitoring marine ecosystems: learning from echinoderms. In: Chen J, Guô C (eds) Ecosystem ecology research trends, Novapublisher (In press)

  41. Tortonese E (1965) Classe Crinoidea. In: Calderini (ed) Fauna d’Italia, vol VI, Bologna, pp 17–35

  42. Vail L (1987) Reproduction in five species of crinoids at Lizard Island, Great Barrier Reef. Mar Biol (Berl) 95:431–446. doi:10.1007/BF00409573

    Article  Google Scholar 

  43. Voogt PA, Dieleman JS (1984) Progesterone and oestrone levels in the gonads and pyloric caeca of the male sea star Asterias rubens: a comparison with the corresponding levels in the female sea star. Comp Biochem Physiol A 79:635–639. doi:10.1016/0300-9629(84)90461-4

    Article  Google Scholar 

  44. Voogt PA, den Besten PJ, Jansen M (1990) The Δ5-pathway in steroid metabolism in the sea star Asterias rubens L. Comp Biochem Physiol 97(B):555–562

    Google Scholar 

  45. Voogt PA, Lambert JGD, Granneman JCM, Jansen M (1992) Confirmation of the presence of oestradiol-17β in sea star Asterias rubens by GC-MS. Comp Biochem Physiol B 101:13–16. doi:10.1016/0305-0491(92)90151-G

    Article  Google Scholar 

  46. Walker CW (1982) Nutrition of gametes. In: Jangoux M, Lawrence M (eds) Echinoderm nutrition. Balkema, Rotterdam, pp 449–468

    Google Scholar 

  47. Wasson KM, Gower BA, Hines GA, Watts SA (2000) Levels of progesterone, testosterone and estradiol, and androstenedione metabolism in the gonads of Lytechinus variegatus (Echinodermata: Echinoidea). Comp Biochem Physiol 126(C):153–165

    CAS  Google Scholar 

  48. Watts SA, Hines GA, Byrum CA, McClintok JB, Marion KR, Hopkins TS (1994) Tissue- and species-specific variations in androgen metabolism. In: David G, Feral R (eds) Echinoderms through time. Balkema, Rotterdam, pp 155–161

    Google Scholar 

  49. Xu RA, Barker MF (1990) Annual changes in the steroid levels in the ovaries and the pyloric caeca of Sclerasterias mollis during the reproductive cycle. Comp Biochem Physiol A 95:127–133. doi:10.1016/0300-9629(90)90020-S

    Article  Google Scholar 

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Acknowledgments

The present work received financial support from the EU (COMPRENDO Project no EVK1-CT-2002-00129). The authors are grateful to Dr. U. Shulte-Oehlmann for her coordinating activity and to all the partners of the COMPRENDO project for their support and advice. All the experiments carried out are in accord with the current laws of our country. The authors are grateful to the anonymous reviewers for their profitable suggestions and careful revision of the manuscript.

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Correspondence to Alice Barbaglio.

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Barbaglio, A., Biressi, A., Melone, G. et al. Reproductive cycle of Antedon mediterranea (Crinoidea, Echinodermata): correlation between morphology and physiology. Zoomorphology 128, 119 (2009). https://doi.org/10.1007/s00435-008-0079-z

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Keywords

  • Echinoderms
  • Oogenesis
  • Spermatogenesis
  • Testosterone
  • Estradiol