Skip to main content
Log in

Changes in podial skeletons during growth in the echinoid Hemicentrotus pulcherrimus

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

Abstract

A feature of the Echinodermata is the presence of a water vascular system; the tube feet, or podia, are the terminal structure of this system and are an organ used for movement, attachment to a substrate, and feeding. The tube foot possesses calcite skeletons in the sucker (the disk skeleton consisting of rosettes and frames) and basal connective tissue (ossicles); however, details of the skeletal elements have not yet been studied in detail. We analyzed the relationship between morphology and the amount of skeleton in the tube feet and other regions by investigating growth in the echinoid Hemicentrotus pulcherrimus (family Strongylocentrotidae). The tube foot disk skeleton consisted of three or four three skeletal elements in a rosette with some distal projections. Approximately 98% of tube feet ossicles showed a ‘C’ shape, while the remainder exhibited an ‘S’, ‘bow’ or ‘triradiate’ shape (n = 24 sea urchins). The tube feet in the oral region possessed bigger distal skeletons and approximately twice the number of ossicles than those of the lateral and aboral regions. With growth, the diameter of the distal skeleton increased to four skeletal elements in a rosette. The number of ossicles in the tube feet increased significantly with a test diameter up to 20–30 mm, and thereafter decreased, but beyond a test diameter of 35 mm the number of ossicles again increased. These results suggest that test growth may cause the observed fluctuation in the number of tube feet ossicles, and that sea urchins accumulate calcium carbonate in the tube feet skeleton as the test grows.

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
Fig. 7

Similar content being viewed by others

References

  • Anstrom JA, Chin JE, Leaf DS, Parks A (1987) Localization and expression of msp130, a primary mesenchyme lineage-specific cell surface protein of the sea urchin embryo. Development 101:255–265

    Article  CAS  PubMed  Google Scholar 

  • Arakaki Y, Uehara T, Fagoonee I (1998) Comparative studies of the genus Echionmetra from Okinawa and Mauritius. Zool Sci 15:159–168

    Article  CAS  Google Scholar 

  • Benson S, Sucov H, Stephens L, Davidson E, Wilt F (1987) A lineage-specific gene encoding a major matrix protein of the sea urchin embryo spicule. I. Authentication of the cloned gene and its developmental expression. Dev Biol 10:499–506

    Article  Google Scholar 

  • Bronstein O, Kroh A, Tautscher B, Liggins L, Haring E (2017) Cryptic speciation in pan-tropical sea urchins: a case study of an edge-of-range population of Tripneustes from the Kermadec Islands. Sci Rep 7(1):1–16

    Article  CAS  Google Scholar 

  • Connolly DM, Desvignes T, Williamson JE (2017) Influence of body size on tube feet morphology and attachment capacity in the sea urchin Holopneustes purpurascens. Mar Biol 164:223

    Article  Google Scholar 

  • Dubois P, Chen CP (1989) Calcification in echinoderms. In: Jangoux M et al (eds), Echinoderm Studies, vol 3. Balkema, Rotterdam, pp 109–178

  • Fenner DH (1973) The respiratory adaptations of the podia and ampullae of echinoids (Echinodermata). Biol Bull 145:323–339

    Article  Google Scholar 

  • Formery L, Orange F, Formery A, Yaguchi S, Lowe CJ, Schubert M, Croce JC (2020) Neural anatomy of echinoid early juveniles and comparison of nervous system organization in echinoderms. J Comp Neurol 529:1135–1156

    Article  PubMed  Google Scholar 

  • Kitazawa C, Amemiya S (2007) Micromere-derived signal regulates larval left-right polarity during sea urchin development. J Exp Zool 307A:1–14

    Article  Google Scholar 

  • Koehl MAR (1982) Mechanical design of spicule-reinforced connective tissue: stiffness. J Exp Biol 98:39–267

    Article  Google Scholar 

  • Leddy HA, Johnson AS (2000) Walking versus breathing: mechanical differentiation of sea urchin podia corresponds to functional specialization. Biol Bull 198:8–93

    Article  Google Scholar 

  • Märkel K (1975) Wachsum des coonarskeletes von Paracentrotus lividus Lmk. (Echinodermata, Echinoidea). Zoomorphologie 82:259–280

    Article  Google Scholar 

  • Morris VB (2009) On the sites of secondary podia formation in a juvenile echinoid: growth of the body types in echinoderms. Dev Genes Evol 219(11–12):597–608

    Article  PubMed  Google Scholar 

  • Mortensen TH (1943) III. 3 Camarodonta. II. Echinidæ, Strongyocentrotidæ, Parasaleniidæ, Echinometridæ. A monograph of the echinoidea. C. A. Reitzel publisher, Copenhagen, pp 248–254

    Google Scholar 

  • Nichols D (1961) A comparative histological study of the tube-feet of two regular echinoids. Q J Micro Sci 102:157–189

    Google Scholar 

  • Nichols D (1967) Chapter 9 Functional morphology of the water-vascular system. In: Boolootian RA (ed) Physiology of Echinodermata. Interscience Publishers, New York

    Google Scholar 

  • Noguchi M (1978) Chapter 4 Metamorphosis of sea urchins. In: Japanese society of developmental biologists (eds) Biology of Metamorphosis. Iwanami-shoten, Tokyo, pp 89–115 (in Japanese)

  • O’loughlin PM, Tavancheh E, Harding C (2016) The Discovery expedition sea cucumbers (Echinodermata: Holothuroidea). Memoirs Museum Victoria 75:53–70

    Article  Google Scholar 

  • O’loughlin PM, Mackenzie M, Vandenspiegel D, (2013) New sea cucumber species from the seamounts on the Southwest Indian Ocean ridge (Echinodermata: Holothuroidea: Aspidochirotida, Elasipodida, Dendrochirotida). Memoirs Museum Victoria 70:37–50

    Article  Google Scholar 

  • Ocana Martin A, Tierno de Figueroa JM, Palomino-Morales RJ (2006) Sclerites in different tissue of mediterranean echinodermata. Zool Sci 23:557–564

    Article  Google Scholar 

  • Okazaki K (1975) Normal development to metamorphosis. In: Cihak G (ed) The sea urchin embryo Biochemistry and Morphogenesis. Springer-Verlag, Berlin Heidelberg, New York, pp 178–232

    Google Scholar 

  • Ruppert EE, Barnes RD (1994) 18 Echinoderms. Invertebrate Zoology. Harcourt Brace college publisher, New York, pp 920–995

    Google Scholar 

  • Seilacher A (1979) Constructional morphology of sand dollars. Paleobiology 5(3):191–221

    Article  Google Scholar 

  • Smith A (2005) Growth and form in echinoids: The evolutionary interplay of plate accretion and plate addition. In: Briggs DEG (ed) Evolving Form and Function: Fossils and Development. Yale Peabody Museum, New Haven

    Google Scholar 

  • Stricker SA (1985) The ultrastructure and formation of the calcareous ossicles in the body wall of the sea cucumber Leptosynapta clarki (Echinodermata, Holothuroida). Zoomorph 105:209–222

    Article  Google Scholar 

  • Thompson JR, Paganos P, Benvenuto G, Arnone MI, Oliveri P (2021) Post-metamorphic skeletal growth in the sea urchin Paracentrotus lividus and implications for body plan evolution. EvoDevo 12:3. https://doi.org/10.1186/s13227-021-00174-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woo SP, Yasin Z, Tan SH, Kajihara H, Fujita T (2015) Sea cucumbers of the genus Stichopus Brandt, 1835 (Holothuroidea, Stichopodidae) in straits of Malacca with description of a new species. ZooKeys 545:1–26

    Article  Google Scholar 

  • Woodland W (1906) Studies I spicule formation. IV. The scleroblastic development of the spicules in Cucumariidae; with a note relating to the plate-and-anchor spicules of Synapta inhaerens. Quart J Micr Sci 49:533–559

    Google Scholar 

  • Woodland W (1907a) Studies in spicule formation. V. The scleroblastic development of the spicules in Ophiuroidea and Echinoidea, and in the genera Antedon and Synapta. Quart J Micr Sci 51:31–43

    Google Scholar 

  • Woodland W (1907b) Studies in spicule formation. VII. The scleroblastic development of the plate-and-anchor spicules of Synapta, and of the wheel spicules of the auricularia larva. Quart J Micr Sci 51:483–509

    Google Scholar 

  • Wray GA, Kitazawa C, Miner B (2004) Chapter 4. Culture of echinoderm larvae through metamorphosis. Meth Cell Biol 74:75–86

    Article  Google Scholar 

Download references

Acknowledgements

We thank Drs. David McClay and Shonan Amemiya for gift of Ig8, Dr. M. Watanabe for presenting experimental tools and students in our laboratories for suggestion and collecting organisms. We also thank the department of fishery in Yamaguchi Prefecture and Yamaguchi Fisheries Cooperative Association for permission to collect sea urchins. This work was supported in part by Marine Invertebrates Research Institute Foundation to C. K.

Author information

Authors and Affiliations

Authors

Contributions

S.K. and C.K. wrote the main manuscript text and prepared all figures and tables. A.Y. and S.K. experimented immunological works. All authors reviewed the manuscript.

Corresponding author

Correspondence to Chisato Kitazawa.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 20 KB)

Supplementary file2 (DOCX 21 KB)

Supplementary file3 (DOCX 18 KB)

435_2022_585_MOESM4_ESM.tif

Supplementary Fig. S1 Changes in the diameter of the tube foot disk skeleton during test growth in Hemicentrotus pulcherrimus. The graphs show the diameter of disk skeletons in tube feet collected from the oral (a), inner oral (b), outer oral (c), lateral (d), and aboral (e) regions. The x-axis and y-axis respectively, show the test diameter and the mean diameter of sucker skeletons of tube feet in specimens grouped by 5-mm size intervals (test diameter), based on data used for Fig. 3. (TIF 79 KB)

435_2022_585_MOESM5_ESM.tif

Supplementary Fig. S2 Changes in the number of tube foot ossicles and the weight and size of the test skeleton during growth in Hemicentrotus pulcherrimus. Graphs (a–e) show the average number of tube foot ossicles collected from the oral (a), inner oral (b), outer oral (c), lateral (d), and aboral (e) regions in relation to test growth. The x-axis and y-axis, respectively, show the test diameter and the mean number of tube foot ossicles in specimens grouped by 5-mm size intervals (test diameter), based on data used for Supplementary Fig. S1. Graph (f) shows changes in the weight of the test skeleton during growth. The dashed line represents the approximate curve. (TIF 84 KB)

435_2022_585_MOESM6_ESM.tif

Supplementary Fig. S3 X-Y scatter between the mean weight of the test skeleton and the mean number of tube foot ossicles (based on the table below). The data of test weight are independent from specimen A–X and the data of mean number of tube foot ossicles are based on the total of Supplementary Table 2. The gray dot line shows the approximate straight line. (TIF 58 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kawasaki, S., Yamanaka, A. & Kitazawa, C. Changes in podial skeletons during growth in the echinoid Hemicentrotus pulcherrimus. Zoomorphology 142, 63–75 (2023). https://doi.org/10.1007/s00435-022-00585-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-022-00585-1

Keywords

Navigation