Skip to main content
Log in

Development of the brittle star Ophiothrix exigua Lyman, 1874 a species that bypasses early unique and typical planktotrophic ophiopluteus stages

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

Abstract

The development of Ophiothrix exigua from spawning through metamorphosis was studied by light and scanning electron microscopy. When some ripe males and females were kept in the same container and subjected to cycles of temperature and light shock, males released sperm, and then, females spawned eggs. After release, spermatozoa survived for approximately 28 h at 24 °C. After fertilization, the egg surface changed from smooth to wrinkled, and then, the fertilized eggs produced polar bodies. After the wrinkles disappeared, the eggs started to cleave holoblastically and equally. The arrangement of blastomeres was irregular after the third cleavage. The embryonic surface developed a thick hyaline layer, and blastomeres were connected to each other by projections and filopodia. After the wrinkled blastula stage, embryos hatched and primary mesenchyme cell ingression occurred. At the initiation of gastrulation, embryos formed tetraradiate spicules and then became typical planktotrophic ophioplutei with four pairs of larval arms. The larvae developed coelomic pouches on their left and right sides, and the pouches divided into anterior and posterior parts. After the left anterior pouch formed a hydropolic lobe, the larvae resorbed all inner larval arms except for the posterolateral arms and then formed an adult rudiment. Finally, juveniles released the pair of posterolateral arms and completed metamorphosis. Our findings indicate that larval development (typical planktotrophic ophioplutei until metamorphosis) of O. exigua is similar to that of other Ophiothrix species, but early development is modified involving the formation of the wrinkled eggs and blastulae.

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

Similar content being viewed by others

References

  • Balser EJ (1998) Cloning by ophiuroid echinoderm larvae. Biol Bull 194:187–193

    Article  Google Scholar 

  • Brooks WK, Grave C (1899) Ophiura brevispina. Mem Natl Acad Sci 8:79–100

    Google Scholar 

  • Byrne M, Selvakumaraswamy P (2006) Chapter 25 phylum Echinodermata: Ophiuroidea. In: Young CM (ed) Atlas of marine invertebrate larvae. Academic press, Burlington, pp 481–498

    Google Scholar 

  • Cerra A, Byrne M (1995) Cellular events of wrinkled blastula formation and the influence of the fertilization envelope on wrinkling in the sea star Patiriella exigua. Acta Zool 76:155–165

    Article  Google Scholar 

  • Cisternas P, Byrne M (2005) Evolution of abbreviated development in the ophiuroid Ophiarachnella gorgonian involved heterochronies and deletions. Can J Zool 83:1067–1078

    Article  Google Scholar 

  • Cisternas P, Byrne M, Selvakumaraswamy P (2004) Evolution of development and the Ophiuroidea—revisited. In: Heinzeller T, Nebelsick JH (eds) Echinoderms. Lisse, München, pp 521–526

    Google Scholar 

  • Deheyn D, Alva V, Jangoux M (1996) Fine structure of the photogenous areas in the bioluminescent ophiuroid Amphipholis squamata (Echinodermata, Ophiuridea). Zoomorphology 116:195–204

    Article  Google Scholar 

  • Deheyn D, Mallefet J, Jangoux M (2000a) Evidence of seasonal variation in bioluminescence of Amphipholis squamata (Ophiuroidea, Echinodermata): effects of environmental factors. J Exp Mar Biol Ecol 245:245–264

    Article  PubMed  Google Scholar 

  • Deheyn D, Mallefet J, Jangoux M (2000b) Cytological changes during bioluminescence production in dissociated photocytes from the ophiuroid Amphipholis squamata (Echinodermata). Cell Tissue Res 299:115–128

    Article  CAS  PubMed  Google Scholar 

  • Fenaux L (1963) Note préliminarie sur le dévelopment larvaire de Amphiura chiajei (Forbes). Vie et Milieu 14:91–96

    Google Scholar 

  • Fenaux L (1969) Le development larvaire chez Opioderma longicauda (Retzius). Ch Biol Mar 10:59–62

    Google Scholar 

  • Fujita T (2000) 32. Phylum Echinodermata. In: Hirayama Y (ed) Diversity and evolution of invertebrates. Tokyo, Shokabo, pp 238–252 (in Japanese)

    Google Scholar 

  • Fukushi T (1960) The external features of the development of the sea urchin, Glyptocidaris crenularis A. Agassiz Bull Mar Biol Stn Asamushi 10:57–63

    Google Scholar 

  • Gilbert SF, Raunio AM (1997) Embryology: constructing the organism. Sinauer Associates, Sunderland

    Google Scholar 

  • Grave C (1903) On the occurrence among echinoderms of larvae with cilia arranged in transverse rings, with a suggestion as to their significance. Biol Bull 5:169–186

    Article  Google Scholar 

  • Guille A (1964) Contribution a l’étude de la systématique et de l’écologie d’Ophiothrix quinquemaculata d. Ch. Vie et Milieu 15:243–301

    Google Scholar 

  • Hendler G (1978) Development of Amphioplus abditus (Verrill) (Echinodermata: Ophiuroidea). II. Description and discussion of ophiuroid skeletal ontogeny and homologies. Biol Bull 154:79–95

    Article  Google Scholar 

  • Hendler G (1982) An echinoderm vitellaria with a bilateral larval skeleton: evidence for the evolution of ophiuroid vitellariae from ophioplutei. Biol Bull 163:431–437

    Article  Google Scholar 

  • Henry JJ, Wray GA, Raff RA (1991) Mechanism of an alternate type of echinoderm blastula formation: the wrinkled blastula of the sea urchin Heliocidaris erythrogramma. Develop Growth Differ 33:317–328

    Article  Google Scholar 

  • Irimura S (1995) 24. Echinodermata: 24-B. Asterozoa: Ophiuroidea. In: Nishimura S (ed) Guide to seashore animals of Japan with color pictures and keys Vol. II. Hoikusha, Osaka, pp 529–537 (in Japanese)

  • Kanatani H (1969) Induction of spawning and oocyte maturation by 1-methyladenine in starfishes. Exp Cell Res 57:333–337

    Article  CAS  PubMed  Google Scholar 

  • Kitazawa C, Nishimura H, Yamaguchi T, Nakano M, Yamanaka A (2009) Novel morphological traits in the early developmental stages of Temnopleurus toreumaticus. Biol Bull 217:215–221

    PubMed  Google Scholar 

  • Kitazawa C, Tsuchihashi Y, Egusa Y, Genda T, Yamanaka A (2010) Morphogenesis during early development in four Temnopleuridae sea urchins. Information 13(3B):1075–1089

    Google Scholar 

  • Kitazawa C, Kobayashi C, Kasahara M, Takuwa Y, Yamanaka A (2012) Morphogenesis of adult traits during the early development of Mespilia globulus Linnaeus, 1758 (Echinodermata: Echinoidea). Zool Stud 51(8):1481–1489

    Google Scholar 

  • Kluge B, Lehmann-Greif M, Fischer A (1995) Longlasting exocytosis and massive structural reorganisation in the egg periphery during cortical reaction in Platynereis dumerilii (Annelida, Polychaeta). Zygote 3:141–156

    Article  CAS  PubMed  Google Scholar 

  • Komatsu M, Shōsaku T (1993) Development of the brittle star Ophioplocus japonicus HL Clark I. Zool Sci 10:295–306

    Google Scholar 

  • MacBride EW (1907) The development of Ophiothrix fragilis. Quart J micr Sci 51:557–606

    Google Scholar 

  • McEward LR, Miner BG (2001) Larval and life-cycle patterns in echinoderms. Can J Zool 79:1125–1170

    Article  Google Scholar 

  • Millott N (1966) Chapter 20 light production. In: Boolootian RA (ed) Physiology of Echinodermata. Interscience Publishers, New York, pp 487–501

    Google Scholar 

  • Mladenov PV (1979) Unusual lecithotrophic development of the Caribbean brittle star Ophiothrix oerstedi. Mar Biol 55:55–62

    Article  Google Scholar 

  • Mladenov PV (1985a) Development and metamorphosis of the brittle star Ophiocoma pumila: evolutionary and ecological implications. Biol Bull 168:285–295

    Article  Google Scholar 

  • Mladenov PV (1985b) Observations on reproduction and development of the Caribbean brittle star Ophiothrix suensoni (Echinodermata: Ophiuroidea) evolutionary and ecological implications. Bull Mar Sci 36:384–388

    Google Scholar 

  • Morgan R, Jangoux M (2004) Juvenile-adult relationship in the gregarious ophiuroid Ophiothrix fragilis (Echinodermata): a behavioral and morphological study. Mar Biol 145:265–276

    Article  Google Scholar 

  • Morgan R, Jangoux M (2005) Larval morphometrics and influence of adults on settlement in the gregarious ophiuroid Ophiothrix fragilis (Echinodermata). Biol Bull 208:92–99

    Article  PubMed  Google Scholar 

  • Mortensen TH (1921) Studies of the developmental and larval forms of echinoderms. GEC Gad, Copenhagen

    Book  Google Scholar 

  • Mortensen TH (1931) Contributions to the study of the development and larval forms of echinoderms I–II. D Kgl Danske Vidensk Selsk Skrifter Naturv Og Math 7:1–65

    Google Scholar 

  • Mortensen TH (1937) Contributions to the study of the development and larval forms of echinoderms II. D Kgl Danske Vidensk Selsk Skrifter Naturv Org Math 7:1–65

    Google Scholar 

  • Mortensen T (1938) Contributions to the study of the development and larval forms of echinoderms. IV. K Dansk Vidensk Selsk 7(3):1–59

    Google Scholar 

  • Nakamura S, Mikamori M, Hiramatsu M, Eura S, Takamoto H, Watanabe M (2001) Spectacular fluorescence emission in sea urchin larvae. Zool Sci 18:807–810

    Article  Google Scholar 

  • Olsen H (1942) The development of the brittle-star Ophiopholis aculeata (O. Fr. Müller). Bergens Mus Årb Naturvidens Rek 6:1–107

    Google Scholar 

  • Selvakumaraswamy P, Byrne M (2000a) Vestigial ophiopluteal structures in the lecithotrophic larvae of Ophionereis schayeri (Ophiuroidea). Biol Bull 198:379–386

    Article  CAS  PubMed  Google Scholar 

  • Selvakumaraswamy P, Byrne M (2000b) Reproduction, spawning, and development of 5 ophiuroids from Australia and New Zealand. Invertebr Biol 119:394–402

    Article  Google Scholar 

  • Selvakumaraswamy P, Byrne M (2006) Evolution of larval form in ophiuroids: insights from the metamorphic phenotype of Ophiothrix (Echinodermata: Ophiuroidea). Evol Dev 8:183–190

    Article  PubMed  Google Scholar 

  • Sewell MA, Young CM (1997) Are echinoderm egg size distributions bimodal? Biol Bull 193:297–305

    Article  Google Scholar 

  • Stancyk SE (1973) Development of Ophiolepis elegans (Echinodermata: Ophiuroidea) and its implications in the estuarine environment. Mar Biol 21:7–12

    Article  Google Scholar 

  • Strathmann RR, Rumrill SS (1987) Phylum Echinodermata, class Ophiuoidea. In: Strathmann MF (ed) Reproduction and development of marine invertebrates of the Northern Pacific Coast. University of Washington Press, Seattle, pp 556–573

    Google Scholar 

  • Thorson G (1946) Reproduction and larval development of Danish marine bottom invertebrates, with special reference to the planktonic larvae in the sound (Ø resund). 12. Echinodermata. Medd Komm Havunders Hjob Plankton 4:343–367

    Google Scholar 

  • Tominaga H, Nakamura S, Komatsu M (2004) Reproduction and development of the conspicuously dimorphic brittle star Ophiodaphne formata (Ophiuroidea). Biol Bull 206:25–34

    Article  PubMed  Google Scholar 

  • Yamashita M (1983) Electron microscopic observations during monospermic fertilization process of the brittle-star Amphipholis kochii Lütken. J Exp Zool 228:109–120

    Article  Google Scholar 

  • Yamashita M (1985) Embryonic development of the brittle-star Amphipholis kochii in laboratory culture. Biol Bull 169:131–142

    Article  Google Scholar 

  • Yamashita M, Iwata F (1988) 15-C Ophiuroids. In: Dan K, Sekiguchi K, Ando H, Watanabe H (eds) Development of invertebrates II. Baihukan, Tokyo, pp 357–367 (in Japanese)

    Google Scholar 

Download references

Acknowledgments

We thank Dr. M. Noguchi for providing of algae and students in our laboratories for collecting of animals and suggestion. We appreciate T. Baba, T. Fujii and C. Miyahara for animal collecting and discussion. We also thank the department of fishery in Yamaguchi Prefecture and Yamaguchi Fisheries Cooperative Association for permission to collect sea urchins. This work was financially supported in part by Yamaguchi University Foundation, JSPS KAKENHI Grant Number 24770227 and from Narishige Zoological Science Award to C. K.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chisato Kitazawa.

Additional information

Communicated by Andreas Schmidt-Rhaesa.

Sae Akahoshi and Sinya Sohara have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kitazawa, C., Akahoshi, S., Sohara, S. et al. Development of the brittle star Ophiothrix exigua Lyman, 1874 a species that bypasses early unique and typical planktotrophic ophiopluteus stages. Zoomorphology 134, 93–105 (2015). https://doi.org/10.1007/s00435-014-0233-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-014-0233-8

Keywords

Navigation