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Metamorphosis and definitive organogenesis in the holothurian Apostichopus japonicus

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Abstract

The structure of the late doliolaria, pentactula and 1-month-old juvenile of the holothurian Apostichopus japonicus was studied using light microscopy and 3D reconstruction methods. It was shown that metamorphosis in this species consists in the reorganization of the shape of the body and the destruction of provisional organs. The late doliolaria has a spindle-like form, ciliary rings and hyaline spheres shifted relative to the anterior-posterior axis of the body. Some provisional organs (ciliary rings, hyaline spheres) are destroyed during settlement, and others (hydropore and hydroporic canal) remain after metamorphosis. Definitive organogenesis in A. japonicus begins long before metamorphosis. The late doliolaria already has well-developed water-vascular and digestive systems, and the ectoneural part of the nervous system. Muscle and hemal systems begin to form in the pentactula. Moreover, the calcareous ring and connective tissue part of the body wall develop at this stage. The pentactula has anlages of the hyponeural part of the nervous system, which form in the mid-ventral and dorsal nerve cords. The hemal ring of the pentactula is located on the inner wall of the water-vascular ring. It remains unclosed in the left ventral radius. One-month-old juveniles have all the major organ systems except respiratory and reproductive systems. The hemal vessels of the intestine are well developed and begin to form the rete mirabile. Differentiation of the intestine into regions due to differential specialization of the enterocytes begins in 1-month-old juveniles. Obviously, emergence of new types of enterocytes enables the animal to consume a wider range of food items and indicates its increased feeding activity.

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References

  • Brusca RC, Brusca GJ (2003) Invertebrates, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Byrne M (1986) The ultrastructure of the morula cells of Eupentacta quenquesemita (Echinodermata: Holothuroidea) and their role in the maintenance of the extracellular matrix. J Morphol 188:179–189

    Article  Google Scholar 

  • Cobb JLS (1995) The nervous systems of Echinodermata: recent results and new approaches. In: Breidbach O, Kutsch W (eds) The nervous systems of invertebrates: an evolutionary and comparative approach. Birkhäuser, Berlin, pp 407–424

    Chapter  Google Scholar 

  • Conand C (2008) Population status, fisheries and trade of sea cucumbers in Africa and the Indian Ocean. In: Toral -Granda V, Lovatelli A, Vasconcellos M (eds) Sea cucumbers. A global review of fisheries and trade. FAO Fisheries and Aquaculture Technical Paper. No. 516. FAO, Rome, pp 143–193

  • Dautov SS (1997) Structure and properties of hyaline spheres in holothuroid larvae. Invertebr Reprod Dev 32:155–161. doi:10.1080/07924259.1997.9672617

    Article  CAS  Google Scholar 

  • Dautov SS, Kashenko SD (1995) Hyaline spheres in auricularia of Stichopus japonicus. Invertebr Reprod Dev 27:61–64

    Article  Google Scholar 

  • Dietrich HF, Fontaine AR (1975) A decalcification method for ultrastructure of echinoderm tissues. Stain Technol 50:351–354

    Article  CAS  PubMed  Google Scholar 

  • Dolmatov IY, Ivantey VA (1993) Histogenesis of longitudinal muscle bands in holothurians. Russ J Dev Biol 24:67–72

    Google Scholar 

  • Dolmatov IY, Mashanov VS (2007) Regeneration in holothurians. Dalnauka, Vladivostok

    Google Scholar 

  • Dolmatov IY, Mokretsova ND (1995) Morphology of pentactula Cucumaria japonica (Dendrochirota, Holothuroidea). Zoologicheskiy zhurnal 74:83–91

    Google Scholar 

  • Dolmatov IY, Yushin VV (1993) Larval development of Eupentacta fraudatrix (Holothuroidea, Dendrochirota). Asian Mar Biol 10:125–134

    Google Scholar 

  • Dolmatov IY, Mashanov VS, Zueva OR (2007) Derivation of muscles of the Aristotle’s lantern from coelomic epithelia. Cell Tissue Res 327:371–384

    Article  PubMed  Google Scholar 

  • Dolmatov IY, Frolova LT, Zakharova EA, Ginanova TT (2011) Development of respiratory trees in the holothurian Apostichopus japonicus (Aspidochirotida: Holothuroidea). Cell Tissue Res 346:327–338

    Article  PubMed  Google Scholar 

  • Drozdov AL, Kornienko ES, Kruchkova GA (1990) Oocyte maturation, development and metamorphosis in the Far eastern sea cucumber. Sov J Mar Biol 16:347–355

    Google Scholar 

  • García-Arrarás JE, Dolmatov IY (2010) Echinoderms: potential model systems for studies on muscle regeneration. Curr Pharm Des 16:942–955

    Article  PubMed  PubMed Central  Google Scholar 

  • Herreid CF, LaRussa VF, DeFesi CR (1976) Blood vascular system of the sea cucumber, Stichopus moebii. J Morphol 150:423–451

    Article  Google Scholar 

  • Herreid CF, Defesi CR, Larussa VF (1977) Vascular follicle system of the sea cucumber Stichopus moebii. J Morphol 154:19–37

    Article  Google Scholar 

  • Hyman LH (1955) The invertebrates: Echinodermata. The coelome Bilateria. McGraw-Hill Book Co., New York

    Google Scholar 

  • Ivanova-Kazas OM (1978) Comparative embryology of invertebrates. Echinodermata and Hemichordata, Nauka

    Google Scholar 

  • Malakhov VV, Cherkasova IV (1991) The embryonal and early larval development of Stichopus japonicus var. armatus (Aspidochirota, Stichopodidae). Zool Zh 70:55–67

    Google Scholar 

  • Malakhov VV, Cherkasova IV (1992) Metamorphosis of the sea cucumber Stichopus japonicus (Aspidochirota, Stichopodidae). Zool Zh 71:11–21

    Google Scholar 

  • Mashanov VS, Dolmatov IY (2000) Developmental morphology of a holothurian Cucumaria japonica (Dendrochirota, Holothuroidea), a species with accelerated metamorphosis. Invertebr Reprod Dev 37:137–146. doi:10.1080/07924259.2000.9652412

    Article  Google Scholar 

  • Mashanov VS, Zueva OR, Heinzeller T, Aschauer B, Dolmatov IY (2007) Developmental origin of the adult nervous system in a holothurian: an attempt to unravel the enigma of neurogenesis in echinoderms. Evol Dev 9:244–256

    Article  PubMed  Google Scholar 

  • McEuen FS, Chia F-S (1991) Development and metamorphosis of two psolid sea cucumbers, Psolus chitonoides and Psolidium bullatum, with a review of reproductive patterns in the family Psolidae (Holothuroidea: Echinodermata). Mar Biol 109:267–279

    Article  Google Scholar 

  • Menton DN, Eisen AZ (1973) Cutaneous wound healing in the sea cucumber, Thyone briareus. J Morphol 141:185–203. doi:10.1002/jmor.1051410206

    Article  CAS  PubMed  Google Scholar 

  • Nakano H, Murabe N, Amemiya S, Nakajima Y (2006) Nervous system development of the sea cucumber Stichopus japonicus. Dev Biol 292:205–212

    Article  CAS  PubMed  Google Scholar 

  • Podkorytov AG, Maslennikov SI (2015) The distribution of the far eastern trepang Apostichopus japonicus (Selenka, 1867) in the open aquatic area of Amur Bay (Sea of Japan) in terms of commercial load. Water Chem Ecol (9):49–57

  • Purcell SW (2010) Managing sea cucumber fisheries with an ecosystem approach. FAO Fisheries and Aquaculture Technical Paper. No. 520. FAO, Rome

  • Purcell SW, Samyn Y, Conand C (2012) Commercially important sea cucumbers of the world. FAO species catalogue for fishery purposes. No. 6. FAO, Rome

  • San Miguel-Ruiz JE, García-Arrarás JE (2007) Common cellular events occur during wound healing and organ regeneration in the sea cucumber Holothuria glaberrima. BMC Dev Biol 7:115. doi:10.1186/1471-213X-7115

    Article  PubMed  PubMed Central  Google Scholar 

  • Smiley S (1986) Metamorphosis of Stichopus californicus (Echinodermata: Holothuroidea) and its phylogenetic implications. Biol Bull 171:611–631

    Article  Google Scholar 

  • Smiley S (1994) Holothuroidea. In: Harrison FW, Chia FS (eds) Microscopic anatomy of invertebrates, vol 14., EchinodermataWiley-Liss Inc, New York, pp 401–471

    Google Scholar 

  • Smiley S, McEuen FS, Chaffee C, Krishnan S (1991) Echinodermata: Holothuroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates, vol 6., BoxwoodPacific Grove, CA, pp 633–750

    Google Scholar 

  • Uthicke S, Byrne M, Conand C (2010) Genetic barcoding of commercial Bêche-de-mer species (Echinodermata: Holothuroidea). Mol Ecol Resour 10:634–646

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Hamel J-F, Mercier A (2015) The sea cucumber Apostichopus japonicus. History, Biology and Aquaculture. Elsevier, Amsterdam

    Google Scholar 

  • Yoshida W, Tamai A, Yanaka T, Ishida S (2002) Normal development and artificial breeding of sea cucumber (Stichopus japonicus Selenka) from Mutsu Bay. Bull Fac Agric Life Sci Hirosaki Univ 4:16–23

    Google Scholar 

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Acknowledgments

The authors express their gratitude to two anonymous reviewers for the valuable comments, which enabled us to improve the quality of the paper. This study was supported by the Russian Science Foundation (Grant. 14-50-00034).

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Correspondence to Igor Yu. Dolmatov.

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Communicated by A. Schmidt-Rhaesa.

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Dolmatov, I.Y., Ginanova, T.T. & Frolova, L.T. Metamorphosis and definitive organogenesis in the holothurian Apostichopus japonicus . Zoomorphology 135, 173–188 (2016). https://doi.org/10.1007/s00435-015-0299-y

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