Skip to main content
SpringerLink
Log in

Cnidarian Larvae: True Planulae, Other-Than-Planulae, and Planulae That Don’t Look Like Planulae

  • REVIEWS
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The life cycle of the common ancestor of Metazoa is a widely debated topic in EvoDevo. This is intimately linked to a number of questions, such as how the larva appeared in the metazoan life cycle and which larval form can be considered ancestral. To approach these questions, we can analyse the life cycles and larval forms of Cnidaria, the basal metazoans that form a sister group to the Bilateria. Almost all cnidarians have a pelagic larva in their life cycle. These larvae are commonly referred to as “planula,” with few exceptions. The planula is a ciliated lecithotrophic larva with epithelial ectoderm and endoderm, a gastric cavity, and an elongated body. The review examines whether the larvae of various Cnidaria fit this description and explores which larval form is ancestral for different cnidarian taxa. It also highlights the enormous diversity of cnidarian larvae, which is still underestimated, and infers the relationship between the evolution of life cycles, reproductive patterns, and larval forms in various phylogenetic groups of cnidarians.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.
Fig. 11.
Fig. 12.
Fig. 13.
Fig. 14.
Fig. 15.
Fig. 16.
Fig. 17.
Fig. 18.
Fig. 19.

REFERENCES

  1. Allman, G.J., A Monograph on the Gymnoblastic or Tubularian Hydroids. In Two Parts. I, The Hydroida in General, London: Royal Society, 1871.

    Google Scholar 

  2. Annunziata, R. and Arnone, M.I., A dynamic regulatory network explains ParaHox gene control of gut patterning in the sea urchin, Development, 2014, vol. 141, no. 12, pp. 2462–2472.

    Article  CAS  PubMed  Google Scholar 

  3. Avian, M., Rottini sandrini L. oocyte development in four species of scyphomedusa in the northern Adriatic Sea, Hydrobiologia, 1991, vol. 216, pp. 189–195.

    Article  Google Scholar 

  4. Babcock, R.C. and Heyward, A.J., Larval development of certain gamete-spawning scleractinian corals, Coral Reefs, 1986, vol. 5, pp. 111–116.

    Article  Google Scholar 

  5. Babcock, R.C. and Ryland, J.S., Larval development of a tropical zoanthid (Protopalythoa sp.), Invertebr. Reprod. Dev., 1990, vol. 17, no. 3, pp. 229–236.

    Article  Google Scholar 

  6. Badham, C., On a larval actinian parasitic in a rhizostome, J. Cell Sci., 1917, vol. 2, no. 246, pp. 221–229.

    Article  Google Scholar 

  7. Ball, E.E., Hayward, D.C., Bridge, T.C., and Miller, D.J., Acropora—the most-studied coral genus, in Handbook of Marine Model Organisms in Experimental Biology: Established and Emerging, CRC Press, 2021, pp. 173–193.

    Google Scholar 

  8. Bamford, E.E., No. XXIII—Pelagic actiniarian larvae, Trans. Linn. Soc. London, 2nd Ser.: Zool., 1912, vol. 15, no. 3, pp. 395–406.

    Google Scholar 

  9. Ben-David-Zaslow, R. and Benayahu, Y., Biochemical composition, metabolism, and amino acid transport in planula-larvae of the soft coral Heteroxenia fuscescens, J. Exp. Zool., 2000, vol. 287, pp. 401–412.

    Article  CAS  PubMed  Google Scholar 

  10. Benayahu, Y., Reproductive cycle and developmental processes during embryogenesis of Clavularia hamra (Cnidaria, Octocorallia), Acta Zool., 1989, vol. 70, no. 1, pp. 29–36.

    Article  Google Scholar 

  11. Benayahu, Y. and Loya, Y., Surface brooding in the Red Sea soft coral Parerythropodium fulvum fulvum (Forskal, 1775), Biol. Bull., 1983, vol. 165, no. 2, pp. 353–369.

    Article  CAS  PubMed  Google Scholar 

  12. Benayahu, Y. and Loya, Y., Life history studies on the red sea soft coral Xenia macrospiculata Gohar, 1940. II. Planulae shedding and post larval development, Biol. Bull., 1984, vol. 166, no. 1, pp. 44–53.

    Article  Google Scholar 

  13. Benayahu, Y. and Loya, Y.J., Sexual reproduction of a soft coral: synchronous and brief annual spawning of Sarcophyton glaucum (Quoy & Gaimard, 1833), Biol. Bull., 1986, vol. 170, no. 1, pp. 32–42.

    Article  Google Scholar 

  14. Benayahu, Y., Achituv, Y., and Berner, T., Embryogenesis and acquisition of algal symbionts by planulae of Xenia umbellata (Octocorallia: Alcyonacea), Mar. Biol., 1988, vol. 100, pp. 93–101.

    Article  Google Scholar 

  15. Berking, S., Principles of branch formation and branch patterning in Hydrozoa, Int. J. Dev. Biol., 2006, vol. 50, pp. 123–134.

    Article  PubMed  Google Scholar 

  16. Berrill, N.J., Developmental analysis of scyphomedusae, Biol. Rev., 1949, vol. 24, no. 4, pp. 393–409.

    Article  CAS  PubMed  Google Scholar 

  17. Berrill, N.J., Growth and form in gymnoblastic hydroids. V. Growth cycle in Tubularia, J. Morphol., 1952, vol. 90, no. 3, pp. 583–601.

    Article  Google Scholar 

  18. Bocharova, E.S. and Kozevich, I.A., Modes of reproduction in sea anemones (Cnidaria, Anthozoa), Biol. Bull., 2011, vol. 38, pp. 849–860.

    Article  Google Scholar 

  19. Bodo, F. and Bouillon, J., Etude histologique du développement embryonnaire de quelques hydroméduses de Roscoff: Phialidium hemisphaericum (L.), Obelia sp. Péron et Lesueur, Sarsia eximia (Allman), Podocoryne carnea (Sars), Gonionemus vertens Agassiz, Cah. Biol. Mar., 1968, vol. 9, pp. 69–104.

    Google Scholar 

  20. Boosten, M., Sant, C., Da Silva O., Chaffron, S., Guidi, L., and Leclere, L., Loss of the benthic life stage in Medusozoa and colonization of the open ocean, bioRxiv, 2023, p. 2023-02.

  21. Brooke, S. and Young, C.M., Reproductive ecology of a deep-water scleractinian coral, Oculina varicosa, from the southeast Florida shelf, Cont. Shelf Res., 2003, vol. 23, no. 9, pp. 847–858.

    Article  Google Scholar 

  22. Brooks, W.K., The life-history of the hydromedusae: a discussion of the origin of the medusae, and of the significance of metagenesis, Mem. Boston: Soc. Nat. Hist., 1886, vol. 3, pp. 359–430.

    Google Scholar 

  23. Bucher, M., Wolfowicz, I., Voss, P.A., Hambleton, E.A., and Guse, A., Development and symbiosis establishment in the cnidarian endosymbiosis model Aiptasia sp., Sci. Rep., 2016, vol. 6, no. 1, pp. 1–11.

    Article  Google Scholar 

  24. Bunting, M., The origin of the sex-cells in Hydractinia and Podocoryne; and the development of Hydractinia, J. Morphol., 1894, vol. 9, pp. 203–236.

    Article  Google Scholar 

  25. Burmistrova, V.A., Osadchenko, B.V., and Bolshakov, F.V., The embryonic development of thecate hydrozoan Gonothyraea loveni (Allman, 1859), Dev. Growth Differ., 2018, vol. 69, no. 8, pp. 483–501.

    Article  Google Scholar 

  26. Byrum, C.A., An analysis of hydrozoan gastrulation by unipolar ingression, Dev. Biol., 2001, vol. 240, no. 2, pp. 627–640.

    Article  CAS  PubMed  Google Scholar 

  27. Carre, D., Etude du developpement d’Halistemma rubrum (Vogt, 1852) siphonophore physonecte Agalmidae, Cah. Biol. Mar., 1971, vol. 12, no. 1, pp. 77–93.

    Google Scholar 

  28. Carre, C. and Carre, D., Ordre des siphonophores, in Traite de Zoologie. Anatomie, Systematique, Biologie, Grasse, P.-P., Ed., Paris: Masson, 1993, pp. 523–559.

    Google Scholar 

  29. Cartwright, P., Developmental insights into origin of complex colonial hydrozoans, Integr. Comp. Biol., 2003, vol. 43, pp. 82–86.

    Article  PubMed  Google Scholar 

  30. Chadwick-Furman, N.E., Spiegel, M., and Nir, I., Sexual reproduction in the tropical corallimorpharian Rhodactis rhodostoma, Invertebr. Biol., 2000, vol. 119, no. 4, pp. 361–369.

    Article  Google Scholar 

  31. Chari, T., Weissbourd, B., Gehring, J., et al., Whole-animal multiplexed single-cell rna-seq reveals transcriptional shifts across Clytia medusa cell types, Sci. Adv., 2021, vol. 7, no. 48, p. eabh1683.

  32. Chia, F.S., Sea anemone reproduction: patterns and adaptive radiations, in Coelenterate Ecology and Behavior, Boston, MA: Springer US, 1976, рр. 261–270.

    Google Scholar 

  33. Chia, F.S. and Crawford, B., Comparative fine structural studies of planulae and primary polyps of identical age of the sea pen, Ptilosarcus gurneyl, J. Morphol., 1977, vol. 151, no. 1, pp. 131–157.

    Article  PubMed  Google Scholar 

  34. Chia, F.S. and Koss, R., Fine structural studies of the nervous system and the apical organ in the planula larva of the sea anemone Anthopleura elegantissima, J. Morphol., 1979, vol. 160, no. 3, pp. 275–297.

    Article  PubMed  Google Scholar 

  35. Chia, F.S. and Spaulding, J.G., Development and juvenile growth of the sea anemone, Tealia crassicornis, Biol. Bull., 1972, vol. 142, pp. 206–218.

    Article  CAS  PubMed  Google Scholar 

  36. Collins, A.G., Phylogeny of Medusozoa and the evolution of cnidarian life cycles, J. Evol. Biol., 2002, vol. 15, pp. 418–432.

    Article  Google Scholar 

  37. Collins, A.G., Schuchert, P., Marques, A.C., et al., Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models, Syst. Biol., 2006, vol. 55, pp. 97–115.

    Article  PubMed  Google Scholar 

  38. Collins, A.G., Bentlage, B., Lindner, A., et al., Phylogenetics of Trachylina (Cnidaria: Hydrozoa) with new insights on the evolution of some problematical taxa, J. Mar. Biol. Assoc. UK, 2008, vol. 88, no. 8, pp. 1673–1685.

    Article  Google Scholar 

  39. Courtney, R., Browning, S., and Seymour, J., Early life history of the “Irukandji” jellyfish Carukia barnesi, PLoS One, 2016, vol. 11, no. 3, p. e0151197.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Dahan, M. and Benayahu, Y., Embryogenesis, planulae longevity, and competence in the octocoral Dendronephthya hemprichi, Invertebr. Biol., 1998, vol. 117, no. 4, pp. 271–280.

    Article  Google Scholar 

  41. Dalyell, J.G., Rare and Remarkable Animals of Scotland Represented from Living Subjects: With Practical Observations on Their Nature, London, 1847, vol. 1.

  42. von Dassow, G. and Mendes, C.B., Pelagic larval polyclads that practice macrophagous carnivory, Invertebr. Biol., 2022, vol. 141, no. 1, p. e12361.

    Article  Google Scholar 

  43. Duffy, D.J., Plickert, G., Kuenzel, T., Tilmann, W., and Frank, U., Wnt signaling pro-motes oral but suppresses aboral structures in Hydractinia metamorphosis and regeneration, Development, 2010, vol. 137, pp. 3057–3066.

    Article  CAS  PubMed  Google Scholar 

  44. Dunn, D.F., Reproduction of the externally brooding sea anemone Ypiactis prolifera Merrill, 1869, Biol. Bull., 1975, vol. 148, no. 2, pp. 199–218.

    Article  CAS  PubMed  Google Scholar 

  45. Dunn, C.W., Giribet, G., Edgecombe, G.D., and Hejnol., A., Animal phylogeny and its evolutionary implications, Ann. Rev. Ecol., Evol., Syst., 2014, vol. 45, pp. 371–395.

    Article  Google Scholar 

  46. Edwards, D.C. and Moore, C.G., Reproduction in the sea pen Funiculina quadrangularis (Anthozoa: Pennatulacea) from the west coast of Scotland, Estuarine, Coastal Shelf Sci., 2009, vol. 82, no. 1, pp. 161–168.

    Article  Google Scholar 

  47. Evans, N.M., Lindner, A., Raikova, E.V., Collins, A.G., and Cartwright, P., Phylogenetic placement of the enigmatic parasite, Polypodium hydriforme, within the phylum Cnidaria, BMC Evol. Biol., 2008, vol. 8, no. 1, p. 139.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Fabricius, K.K., Octocorallia, in Encyclopedia of Modern Coral Reefs, Hopley, D., Ed., Dordrecht: Springer Science & Business Media, 2011, pp. 740–745.

    Google Scholar 

  49. Fadlallah, Y.H., Sexual reproduction, development and larval biology in scleractinian corals: a review, Coral Reefs, 1983, vol. 2, pp. 129–150.

    Article  Google Scholar 

  50. Fadlallah, Y.H. and Pearse, J.S., Sexual reproduction in solitary corals: overlapping oogenic and brooding cycles, and benthic planulas in Balanophyllia elegans, Mar. Biol., 1982, vol. 71, pp. 223–231.

    Article  Google Scholar 

  51. Farrant, P.A., Gonad development and the planulae of the temperate Australian soft coral Capnella gaboensis, Mar. Biol., 1986, vol. 92, pp. 381–392.

    Article  Google Scholar 

  52. Fautin, D.G. and Mariscal, R.N., Cnidaria: Anthozoa, in Microscopic Anatomy of Invertebrates, Harrison, F.W. and Westfall, J.A., Eds., New York: Wiley-Liss, 1991, vol. 2, pp. 267–358.

    Google Scholar 

  53. Foster, T. and Gilmour, J., Egg size and fecundity of biannually spawning corals at Scott reef, Sci. Rep., 2020, vol. 10, p. 12313. https://doi.org/10.1038/s41598-020-68289-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Freeman, G., Experimental studies on embryogenesis in hydrozoans (Trachylina and Syphonophora) with direct development, Biol. Bull., 1983, vol. 165, pp. 591–618.

    Article  PubMed  Google Scholar 

  55. Galliot, B., Quiquand, M., Ghila, L., De Rosa, R., Milijko-vic-Licina, M., and Chera, S., Origin of neurogenesis, a cnidarian view, Dev. Biol., 2009, vol. 332, pp. 2–24.

    Article  CAS  PubMed  Google Scholar 

  56. Garcia-Cardenas, F.J. and López-Gonzalez, P.J., Some observations on the reproductive biology of the Mediterranean pennatulacean Pteroeides spinosum (Ellis and Solander, 1786) (Cnidaria: Octocorallia: Pennatulacea), Thalassas: Int. J. Mar. Sci., 2023, vol. 39, no. 1, pp. 181–197.

    Article  Google Scholar 

  57. Gemmill, J.F., The development of the sea anemones, Melridium dianthus (Ellis) and Adamsia palliata (Bohad), Philos. Trans. R. Soc. London, B, 1920, vol. 209, pp. 351–375.

    Article  Google Scholar 

  58. Gemmill, J.F., Memoirs: the development of the sea anemone Bolocera tuediae (Johnst), J. Cell Sci., 1921, vol. 2, no. 260, pp. 577–587.

    Article  Google Scholar 

  59. Gilbert, E., Teeling, C., Lebedeva, T., Pedersen, S., Chrismas, N., Genikhovich, G., and Modepalli, V., Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis, Development, 2022, vol. 149, no. 16, p. dev200833.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Gilbert, E., Craggs, J., and Modepalli, V., Gene regulatory network that shaped the evolution of larval sensory organ in Cnidaria, bioRxiv, 2023, p. 2023-09.

  61. Goette, A., Abhandlungen zur Entwickelungsgeschichte der Tiere. Viertes Heft. Entwickelungsgeschichte der Aurelia aurita und Cotylorhiza tuberculata, Hamburg: Verlag von Leoplod Voss, 1887.

    Google Scholar 

  62. Goette, A., Vergleichende Entwicklungsgeschichte von Pelagia noctiluca Per., Z. Wiss. Zool., 1893, vol. 55, pp. 644–695 (pl. 28–31).

  63. Gold, D.A., Nakanishi, N., Hensley, N.M., Hartenstein, V., and Jacobs, D.K., Cell tracking supports secondary gastrulation in the moon jellyfish Aurelia, Dev. Genes Evol., 2016, vol. 226, no. 6, pp. 383–387.

    Article  PubMed  Google Scholar 

  64. Hamel, J.-F., Wareham-Hayes, V.E., and Mercier, A., Reproduction of a bathyal pennatulacean coral in the Canadian Arctic, Deep-Sea Res., Part A, 2020, vol. 162, p. 103321.

    CAS  Google Scholar 

  65. Hanaoka, K.I., Notes on the early development of a stalked medusa, Proc. Imp. Acad. Jpn., 1934, vol. 10, pp. 117–120.

    Article  Google Scholar 

  66. Hein, W., Unteruchungen uber die Entwiclung der Aurelia aurita, Z. Wiss. Zool., 1900, vol. 67, pp. 401–438.

    Google Scholar 

  67. Hein, W., Untersuchungen über die Entwicklung von Cotylorhiza tuberculata, Z. Wiss. Zool., 1903, vol. 73, pp. 302–320.

    Google Scholar 

  68. Helm, R.R., Evolution and development of scyphozoan jellyfish, Biol. Rev., 2018, vol. 93, no. 2, pp. 1228–1250.

    Article  PubMed  Google Scholar 

  69. Helm, R.R., Tiozzo, S., Lilley, M.K., Lombard, F., and Dunn, C.W., Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles, EvoDevo, 2015, vol. 6, no. 1, p. 11.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Heltzel, P. and Babcock, R., Sexual reproduction, larval development and benthic planulae of the solitary coral Monomyces rubrum (Scleractinia: Anthozoa), Mar. Biol., 2002, vol. 140, pp. 659–667.

    Article  Google Scholar 

  71. Hirose, M., Kinzie, R.A., and Hidaka, M., Early development of zooxanthella-containing eggs of the corals Pocillopora verrucosa and P. eydouxi with special reference to the distribution of zooxanthellae, Biol. Bull., 2000, vol. 199, no. 1, pp. 68–75.

    Article  CAS  PubMed  Google Scholar 

  72. Hirose, M., Yamamoto, H., and Nonaka, M., Metamorphosis and acquisition of symbiotic algae in planula larvae and primary polyps of Acropora spp., Coral Reefs, 2008, vol. 27, no. 2, pp. 247–254.

    Article  Google Scholar 

  73. Hirose, M., Obuchi, M., Hirose, E., and Reimer, J.D., Timing of spawning and early development of Palythoa tuberculosa (Anthozoa, Zoantharia, Sphenopidae) in Okinawa, Japan, Biol. Bull., 2011, vol. 220, no. 1, pp. 23–31.

    Article  PubMed  Google Scholar 

  74. Holts, L.J. and Beauchamp, K.A., Sexual reproduction in the corallimorpharian sea anemone Corynactis californica in a central California kelp forest, Mar. Biol., 1993, vol. 116, pp. 129–136.

    Article  Google Scholar 

  75. Holst, S. and Jarms, G., Effects of low salinity on settlement and strobilation of scyphozoa (Cnidaria): is the lion’s mane Cyanea capillata (L.) able to reproduce in the brackish Baltic Sea?, Jellyfish Blooms: New Problems and Solutions, 2010, pp. 53–68.

  76. Holst, S, Kaiser, L.R., and Sötje, I., Planula settlement and polyp morphogenesis in two bloom forming jellyfish species of the genus Cyanea Péron and Lesueur, 1810 and effects of abiotic factors on planulocysts, Mar. Biol., 2024, vol. 171, no. 1, pp. 1–21.

    Article  Google Scholar 

  77. Hyde, I., Entwicklungsgeschichte einiger Scyphomedusen, Z. Wiss. Zool., 1894, vol. 58, pp. 553–563.

    Google Scholar 

  78. Hyman, L.H., The Invertebrates: Protozoa through Ctenophora, New York: McGraw-Hill Book, 1940.

    Google Scholar 

  79. Istock, C.A., The evolution of complex life cycle phenomena: an ecological perspective, Evolution, 1967, pp. 592–605.

  80. Ivanova-Kazas, O.M., Evolyutsionnaya embriologiya zhivotnykh (Evolutionary Embryology of Animals), St. Petersburg: Nauka, 1995.

  81. Jarms, G., Bamstedt, U., Tiemann, H., Martinussen, M.B., Fossa, J.H., and Hoisoeter, T., The holopelagic life cycle of the deep-sea medusa Periphylla periphylla (Scyphozoa, Coronatae), Sarsia, 1999, vol. 84, no. 1, pp. 55–65.

    Article  Google Scholar 

  82. Jarms, G., Tiemann, H., and Bamstedt, U., Development and biology of Periphylla periphylla (Scyphozoa: Coronatae) in a Norwegian fjord, Mar. Biol., 2002, vol. 141, pp. 647–657.

    Article  Google Scholar 

  83. Kahng, S.E., Benayahu, Y., and Lasker, H.R., Sexual reproduction in octocorals, Mar. Ecol.: Prog. Ser., 2011, vol. 443, pp. 265–283.

    Article  Google Scholar 

  84. Kai, T., Reproductive and larval biology of the black coral, Antipathes fiordensis, MS Thesis, 2000. http://hdl.handle.net/10523/14694.

  85. Kakinuma, Y., An experimental study of the life cycle and organ differentiation of Aurelia aurita Lamarck, Bull. Mar. Biol. Stat. Asamushi, 1975, vol. 15, pp. 1–3.

    Google Scholar 

  86. Kaposi, K.L., Courtney, R.L., and Seymour, J.E., A note on the sexual reproductive biology of Ricordea yuma (Corallimorpharia), Coral Reefs, 2023, vol. 42, pp. 755–760.

    Article  Google Scholar 

  87. Kayal, E., Roure, B., Philippe, H., Collins, A.G., and Lavrov, D.V., Cnidarian phylogenetic relationships as revealed by mitogenomics, BMC Evol. Biol., 2013, vol. 13, pp. 1–18.

    Article  Google Scholar 

  88. Kayal, E., Bentlage, B., Pankey, M.S., et al., Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits, BMC Evol. Biol., 2018, vol. 18, p. 68.

    Article  PubMed Central  Google Scholar 

  89. Kikinger, R., Cotylorhiza tuberculata (Cnidaria: Scyphozoa)? Life history of a stationary population, Mar. Ecol., 1992, vol. 13, no. 4, pp. 333–362.

    Article  Google Scholar 

  90. Kikinger, R. and von Salvini-Plawen, L., Development from polyp to stauromedusa in Stylocoronella (Cnidaria: Scyphozoa), J. Mar. Biol. Assoc. UK, 1995, vol. 75, no. 4, pp. 899–912.

    Article  Google Scholar 

  91. Kowalevsky, A., Zur Entwicklungsgeschichte der Lucernaria, Zool. Anz., 1884, vol. 7, pp. 712–717.

    Google Scholar 

  92. Kowalewsky, A., Untersuchungen über die Entwicklung der Coelenteraten, Nachr. Gesellsch. Freunde Naturerkenntniss, Anthrop., und Ethnol., Moskow, 1873.

    Google Scholar 

  93. Krasovec, G., Pottin, K., Rosello, M., Quéinnec, E., and Chambon, J.P., Apoptosis and cell proliferation during metamorphosis of the planula larva of Clytia hemisphaerica (Hydrozoa, Cnidaria), Dev. Dyn., 2021, vol. 250, no. 12, pp. 1739–1758.

    Article  CAS  PubMed  Google Scholar 

  94. Kraus, Yu., Morphomechanical programming of morphogenesis in cnidarian embryos, Int. J. Dev. Biol., 2006, vol. 50, pp. 267–275.

    Article  PubMed  Google Scholar 

  95. Kraus, Y., Inductive activity of the posterior tip of planula in the marine hydroid Dynamena pumila, Russ. J. Dev. Biol., 2011, vol. 42, no. 2, pp. 92–100.

    Article  Google Scholar 

  96. Kraus, Y.A. and Markov, A.V., Gastrulation in Cnidaria: the key to an understanding of phylogeny or the chaos of secondary modifications?, Biol. Bull. Rev., 2017, vol. 7, pp. 7–25.

    Article  Google Scholar 

  97. Kraus, Y., Flici, H., Hensel, K., Plickert, G., Leitz, T., and Frank, U., The embryonic development of the cnidarian Hydractinia echinata, Evol. Dev., 2014, vol. 16, no. 6, pp. 323–338.

    Article  PubMed  Google Scholar 

  98. Kraus, J.E., Fredman, D., Wang, W., et al., Adoption of conserved developmental genes in development and origin of the medusa body plan, EvoDevo, 2015, vol. 6, no. 1, pp. 1–5.

    Article  Google Scholar 

  99. Kraus, Y., Chevalier, S., and Houliston, E., Cell shape changes during larval body plan development in Clytia hemisphaerica, Dev. Biol., 2020, vol. 468, pp. 59–79.

    Article  CAS  PubMed  Google Scholar 

  100. Kraus, Y., Osadchenko, B., and Kosevich, I., Embryonic development of the moon jellyfish Aurelia aurita (Cnidaria, Scyphozoa): another variant on the theme of invagination, PeerJ, 2022, vol. 10, p. e13361.

    Article  PubMed  PubMed Central  Google Scholar 

  101. Kroiher, M., Plickert, G., and Müller, W.A., Pattern of cell proliferation in embryogenesis and planula development of Hydractinia echinata predicts the postmetamorphic body pattern, Rouxs Arch. Dev. Biol., 1990, vol. 199, no. 3, pp. 156–163.

    Article  PubMed  Google Scholar 

  102. Kruger, A. and Schleyer, M.H., Sexual reproduction in the coral Pocillopora verrucosa (Cnidaria: Scleractinia) in Kwazulu-Natal, South Africa, Mar. Biol., 1998, vol. 132, no. 4, pp. 703–710.

  103. Kupaeva, D., Lebedeva, T., Kobrinsky, Z., Vanwalleghem, D., Prudkovsky, A., and Kremnyov, S., Margelopsid species search taxonomic home within Corymorphidae and Boreohydridae, PeerJ, 2023, vol. 11, p. e16265. https://doi.org/10.7717/peerj.16265

    Article  PubMed  PubMed Central  Google Scholar 

  104. Larink, O., Ectopleura sp. proactinula larva Helgoland 2011, Marine Plankton Helgoland, 2011. https://av.tib.eu/media/55440.

  105. Larink, O., Anthozoa planula Helgoland 2014, Marine Plankton Helgoland, 2014. https://av.tib.eu/media/ 55417.

  106. Larink, O., Cerianthus sp. antipathula larva Helgoand 2016, Marine Plankton Helgoland, 2016. https://av.tib.eu/media/55470.

  107. Larson, P., Brooding sea anemones (Cnidaria: Anthozoa: Actiniaria): paragons of diversity in mode, morphology, and maternity, Invertebr. Biol., 2017, vol. 136, no. 1, pp. 92–112.

    Article  Google Scholar 

  108. Larson, P.G., Hamel, J.-F., and Mercier, A., Redescription and notes on the reproductive biology of the sea anemone Urticina fecunda (Verrill, 1899), comb. nov. (Cnidaria: Actiniaria: Actiniidae), Zootaxa, 2012, vol. 3523, pp. 69–79.

    Article  Google Scholar 

  109. Lebedeva, T., Aman, A.J., Graf, T., et al., Cnidarian–bilaterian comparison reveals the ancestral regulatory logic of the β-catenin dependent axial patterning, Nat. Commun., 2021, vol. 12, no. 1, p. 4032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Leclere, L., Copley, R.R., Momose, T., and Houliston, E., Hydrozoan insights in animal development and evolution, Curr. Opin. Genet. Dev., 2016, vol. 39, pp. 157–167.

    Article  CAS  PubMed  Google Scholar 

  111. Leloup, E., Anthozoa: Ceriantharia: Larvae, ICES Identification Leaflets for Plankton, 1962, no. 93. https://doi.org/10.17895/ices.pub.5018

  112. Link, O., Jahnel, S.M., Janicek, K., et al., A cell-type atlas from a scyphozoan jellyfish Aurelia coerulea (formerly sp. 1) provides insights into changes of cell-type diversity in the transition from polyps to medusa, bioRxiv, 2023, p. 2023-08.

  113. Lowe, E., Memoirs: the embryology of Tubularia larynx (Allm.), J. Cell Sci., 1926, vol. 2, no. 280, pp. 599–627.

    Article  Google Scholar 

  114. Maegele, I., Rupp, S., Ozbek, S., Guse, A., Hambleton, E.A., and Holstein, Th.W., A predatory gastrula leads to symbiosis-independent settlement in Aiptasia, bioRxiv, 2023. https://doi.org/10.1101/2023.05.26.542442

  115. Manko, M.K., Munro, C., and Leclère, L., Establishing bilateral symmetry in hydrozoan planula larvae, a review of siphonophore early development, Integr. Comp. Biol., 2023, p. icad081.

  116. Marfenin, N.N. and Kosevich, I.A., Morphogenetic evolution of hydroid colony pattern, Hydrobiologia, 2004, vol. 530/531, pp. 319–327.

    Article  Google Scholar 

  117. Marlow, H., Evolutionary development of marine larvae, in Evolutionary Ecology of Marine Invertebrate Larvae, Carrier, T.J., Reitzel, A.M., and Heyland, A., Eds., Oxford: Oxford Univ. Press, 2018, pp. 16–33.

    Google Scholar 

  118. Marlow, H.Q. and Martindale, M.Q., Embryonic development in two species of scleractinian coral embryos: symbiodinium localization and mode of gastrulation, Evol. Dev., 2007, vol. 9, no. 4, pp. 355–367.

    Article  PubMed  Google Scholar 

  119. Marlow, H., Tosches, M.A., Tomer, R., Steinmetz, P.R., Lauri, A., Larsson, T., and Arendt, D., Larval body patterning and apical organs are conserved in animal evolution, BMC Biol., 2014, vol. 12, no. 1, p. 1741-7007-12-7.

  120. Marques, A.C. and Collins, A.G., Cladistic analysis of Medusozoa and cnidarian evolution, Invert. Biol., 2004, vol. 123, no. 1, pp. 23–42.

    Article  Google Scholar 

  121. Martin, V., Development of nerve cells in hydrozoan planulae. I. Differentiation of ganglionic cells, Biol. Bull., 1988a, vol. 174, pp. 319–329.

    Article  Google Scholar 

  122. Martin, V., Development of nerve cells in hydrozoan planulae: II. Examination of sensory cell differentiation using electron microscopy and immunocytochemistry, Biol. Bull., 1988b, vol. 175, pp. 319–329.

    Article  Google Scholar 

  123. Martin, V.J. and Archer, W.E., Stages of larval development and stem cell population changes during metamorphosis of a hydrozoan planula, Biol. Bull., 1997, vol. 192, no. 1, pp. 41–52.

    Article  CAS  PubMed  Google Scholar 

  124. Martin, V.J. and Chia, F., Ultrastructure of scyphozoan planula Cassiopeia xamachana, Biol. Bull., 1982, vol. 163, pp. 320–328.

    Article  Google Scholar 

  125. Martin, V.J. and Thomas, M.B., Nerve elements in the planula of the hydrozoan Pennaria tiarella, J. Morphol., 1980, vol. 166, no. 1, pp. 27–36.

    Article  PubMed  Google Scholar 

  126. Martindale, M.Q. and Hejnol., A., A developmental perspective: changes in the position of the blastopore during bilaterian evolution, Dev. Cell, 2009, vol. 17, no. 2, pp. 162–174.

    Article  CAS  PubMed  Google Scholar 

  127. Matthews, A., The development of Alcyonium digitatum with some notes on the early colony formation, Q. J. Microsc. Sci., 1917, vol. 62, pp. 43–94.

    Google Scholar 

  128. Matus, D.Q., Thomsen, G.H., and Martindale, M.Q., FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian, Dev. Genes Evol., 2007, vol. 217, no. 2, pp. 137–148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Mayorova, T.D., Kosevich, I.A., and Melekhova, O.P., On some features of embryonic development and metamorphosis of Aurelia aurita (Cnidaria, Scyphozoa), Russ. J. Dev. Biol., 2012, vol. 43, no. 5, pp. 271–285.

    Article  CAS  Google Scholar 

  130. Mayorova, T., Kosevich, I., Dulin, N., Savina, E., and Kraus, Y., Organizer regions in marine colonial hydrozoans, Zoology, 2015, vol. 118, no. 2, pp. 89–101.

    Article  PubMed  Google Scholar 

  131. Mayorova, T.D., Osadchenko, B., and Kraus, Y., How to build a larval body with less than a hundred cells? Insights from the early development of a stalked jellyfish (Staurozoa, Cnidaria), Org. Diversity Evol., 2020, vol. 20, pp. 681–699.

    Article  Google Scholar 

  132. McEdward, L.R. and Janies, D.A., Life cycle evolution in asteroids: what is a larva?, Biol. Bull., 1993, vol. 184, no. 3, pp. 255–268.

    Article  CAS  PubMed  Google Scholar 

  133. McFadden, C.S., van Ofwegen, L.P., and Quattrini, A.M., Revisionary systematics of Octocorallia (Cnidaria: Anthozoa) guided by phylogenomics, Bull. Soc. Syst. Biol., 2022, vol. 1, no. 3. https://doi.org/10.18061/bssb.v1i3.8735

  134. McMurrich, J.P., On the development of the hexactinia, J. Morphol., 1891, vol. 4, pp. 303–330.

    Google Scholar 

  135. Mercier, A., Baillon, S., Daly, M., Macrander, J., and Hamel, J.F., Biology of a deep-water sea anemone (Anthozoa: Actiniidae) from eastern Canada: Spawning, development, and growth, Deep-Sea Res., 2016a, vol. 2. https://doi.org/10.1016/j.dsr2.2016.01.006i

  136. Mercier, A., Sun, Z., Parrish, C.C., and Hamel, J.-F., Remarkable shifts in offspring provisioning during gestation in a live-bearing cnidarian, PLoS One, 2016b, vol. 11, no. 4, p. e0154051.

    Article  PubMed  PubMed Central  Google Scholar 

  137. Metschnikoff, E., Studien uber die Entwicklung der Meduse und Siphonophoren, Z. Wiss. Zool., 1874, vol. 24, pp. 15–80.

    Google Scholar 

  138. Metschnikoff, E., Embryologische Studien an Medusen. Ein Beitrag Zur Genealogie der Primitiv-Organe, Wien: Alfred Hölder, 1886.

    Book  Google Scholar 

  139. Mikhailov, K.V., Konstantinova, A.V., Nikitin, M.A., et al., The origin of Metazoa: a transition from temporal to spatial cell differentiation, BioEssays, 2009, vol. 31, no. 7, pp. 758–768.

    Article  CAS  PubMed  Google Scholar 

  140. Miller, K., Genetic structure of black coral populations in New Zealand’s fiords, Mar. Ecol.: Prog. Ser., 1997, vol. 161, pp. 123–132.

    Article  Google Scholar 

  141. Miranda, L.S., Hirano, Y.M., Mills, C.E., Falconer, A., Fenwick, D., Marques, A.C., and Collins, A.G., Systematics of stalked jellyfishes (Cnidaria: Staurozoa), PeerJ, 2016, vol. 4, p. e1951.

    Article  PubMed  PubMed Central  Google Scholar 

  142. Mizrahi, D., Navarrete, S.A., and Flores, A.A.V., Groups travel further: pelagic metamorphosis and polyp clustering allow higher dispersal potential in sun coral propagules, Coral Reefs, 2014, vol. 33, pp. 443–448.

    Article  Google Scholar 

  143. Molodtsova, T.N., On the taxonomy and presumable evolutionary pathways of planktonic larvae of Ceriantharia (Anthozoa, Cnidaria), in Coelenterate Biology, Fautin, D.G., Westfall, J.A., and Cartwrigh, P., Eds., Dordrecht: Springer, 2003, pp. 261–266.

    Google Scholar 

  144. Molodtsova, T.N. and Malakhov, V.V., Cerianthus lloydii (Anthozoa, Ceriantharia) from the volcanic ecosystem of Kraternaya Bay. 2. Larval development, Hydrobiol. J., 1997, vol. 33, nos. 6–7, pp. 44–51.

    Google Scholar 

  145. Molodtsova, T.N., Opresko, D.M., O’Mahoney, M., et al., One of the deepest genera of Antipatharia: taxonomic position revealed and revised, Diversity, 2023, vol. 15, no. 3, p. 436. https://doi.org/doi.org/10.3390/d15030436

    Article  CAS  Google Scholar 

  146. Momose, T., Derelle, R., and Houliston, E., A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica, Development, 2008, vol. 135, pp. 2105–2113.

    Article  CAS  PubMed  Google Scholar 

  147. Morandini, A.C., Silveira, F.L., and Jarms, G., The life cycle of Chrysaora lactea Eschscholtz, 1829 (Cnidaria, Scyphozoa) with notes on the scyphistoma stage of three other species, Hydrobiologia, 2004, vol. 530, pp. 347–354.

    Article  Google Scholar 

  148. Muller, F., Formverwandlungen der Liriope catharinensis n. sp., Arch. Nat., 1859, vol. 25, no. 1, pp. 310–321.

    Google Scholar 

  149. Muller-Cale, K., Zur Entwicklunggeschichte einiger Thecaphoren, Zool. Jahrbücher. Abt. Anat. Ont. Tiere, 1914, vol. 37, pp. 83–112.

    Google Scholar 

  150. Nakanishi, N., Yuan, D., Jacobs, D.K., and Hartenstein, V., Early development, pattern, and reorganization of the planula nervous system in Aurelia (Cnidaria, Scyphozoa), Dev. Genes Evol., 2008, vol. 218, no. 10, pp. 511–524.

    Article  PubMed  Google Scholar 

  151. Nakanishi, N., Renfer, E., Technau, U., and Rentzsch, F., Nervous systems of the sea anemone Nematostella vectensis are generated by ectoderm and endoderm and shaped by distinct mechanisms, Development, 2012, vol. 139, no. 2, pp. 347–357.

    Article  CAS  PubMed  Google Scholar 

  152. Nawrocki, A.M., Collins, A.G., Hirano, Y.M., Schuchert, P., and Cartwright, P., Phylogenetic placement of hydra and relationships within Aplanulata (Cnidaria: Hydrozoa), Mol. Phylogenet. Evol., 2013, vol. 67, no. 1, pp. 60–71.

    Article  PubMed  Google Scholar 

  153. Nielsen, C., The origin of metamorphosis, Evol. Dev., 2000, vol. 2, no. 3, pp. 127–129.

    Article  CAS  PubMed  Google Scholar 

  154. Nielsen, C., Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic Gastraea?, BMC Evol. Biol., 2013, vol. 13, no. 1, p. 171.

    Article  PubMed  PubMed Central  Google Scholar 

  155. Nordstrom, K., Wallen Seymour, J., and Nilsson, D., A simple visual system without neurons in jellyfish larvae, Proc. R. Soc. London, Ser. B, 2003, vol. 270, no. 1531, pp. 2349–2354.

    Article  Google Scholar 

  156. Nyholm, K.G., Zur Entwicklung und Entwicklungsbiologie der Ceriantharien und Actinien, Zool. Bidrag., Upps., 1942–1944, vol. 22, pp. 87–248.

    Google Scholar 

  157. Nyholm, K.G., Zur entwicklung und Entwicklungsbiologie der Ceriantarien und Actinien, Zool. Bidrag. Upps., 1943, vol. 22, pp. 89–248.

    Google Scholar 

  158. Okamura, B., Gruhl, A., and Reft, A.J., Cnidarian origins of the Myxozoa, in Myxozoan Evolution, Ecology and Development, Okamura, B., Gruhl, A., and Bartholomew, J.L., Eds., Cham: Springer, 2015, pp. 45–68.

    Book  Google Scholar 

  159. Okubo, N., Restructuring the traditional suborders in the order Scleractinia based on embryogenetic morphological characteristics, Zool. Sci., 2016, vol. 33, no. 1, pp. 116–123. https://doi.org/10.2108/zs150094

    Article  Google Scholar 

  160. Okubo, N. and Motokawa, T., Embryogenesis in the reef-building coral Acropora spp., Zool. Sci., 2007, vol. 24, no. 12, pp. 1169–1177.

    Article  Google Scholar 

  161. Okubo, N., Mezaki, T., Nozawa, Y., et al., Comparative embryology of eleven species of stony corals (Scleractinia), PLoS One, 2013, vol. 8, no. 12, p. e84115.

    Article  PubMed  PubMed Central  Google Scholar 

  162. Okubo, N., Hayward, D.C., Foret, S., and Ball, E.E., A comparative view of early development in the corals Favia lizardensis, Ctenactis echinata, and Acropora millepora—morphology, transcriptome, and developmental gene expression, BMC Evol. Biol., 2016, vol. 16, no. 48. https://doi.org/10.1186/s12862-016-0615-2

  163. Opresko, D.M. and Sanchez, J.A., Caribbean shallow-water black corals (Cnidaria: Anthozoa: Antipatharia), Caribb. J. Sci., 2005, vol. 41, no. 3, pp. 492–507.

    Google Scholar 

  164. Osadchenko, B.V. and Kraus, Y.A., Trachylina: the group that remains enigmatic despite 150 years of investigations, Russ. J. Dev. Biol., 2018, vol. 49, no. 3, pp. 134–145.

    Article  Google Scholar 

  165. Otto, J.J., Early development and planula movement in Haliclystus (Scyphozoa: Stauromedusae), in Coelenterate Ecology and Behavior, Mackie, G.O., Ed., Springer, 1976, pp. 319–329.

    Google Scholar 

  166. Otto, J.J., The settlement of Haliclystus planulae, in Settlement and Metamorphosis of Marine Invertebrate Larvae, Chia, F.-S. and Koss, R., Eds., New York: Elsevier, 1978, pp. 13–22.

    Google Scholar 

  167. Payne, F., Further studies on the life history of Craspedacusta ryderi, a fresh-water hydromedusan, Biol. Bull., 1926, vol. 50, no. 6, pp. 433–443.

    Article  Google Scholar 

  168. Pennati, R., Dell’Anna, A., Zega, G., De Bernardi, F., and Piraino, S., Retinoic acid influences antero-posterior positioning of peptidergic neurons in the planula larva of the hydrozoan Clava multicornis, Mar. Ecol., 2013, vol. 34, pp. 143–152.

    Article  CAS  Google Scholar 

  169. Perkins, H.F., The development of Gonionema murbachii, Proc. Acad. Nat. Sci. Philadelphia, 1902, vol. 54, pp. 750–790.

    Google Scholar 

  170. Piovani, L. and Marlétaz, F., Single-cell transcriptomics refuels the exploration of spiralian biology, Brief. Funct. Genomics, 2023, vol. 22, no. 6, pp. 517–524.

    Article  PubMed  PubMed Central  Google Scholar 

  171. Piraino, S., Zega, G., Di Benedetto, C., et al., Complex neural architecture in the diploblastic larva of Clava multicornis (Hydrozoa, Cnidaria), J. Comp. Neurol., 2011, vol. 519, no. 10, pp. 1931–1951.

    Article  PubMed  Google Scholar 

  172. Pitt, K.A., Life history and settlement preferences of the edible jellyfish Catostylus mosaicus (Scyphozoa: Rhizostomeae), Mar. Biol., 2000, vol. 136, pp. 269–279.

    Article  Google Scholar 

  173. Plickert, G., Kroiher, M., and Munck, A., Cell proliferation and early differentiation during embryonic development and metamorphosis of Hydractinia echinata, Development, 1988, vol. 103, no. 4, pp. 795–803.

    Article  CAS  PubMed  Google Scholar 

  174. Plickert, G., Jacoby, V., Frank, U., Muller, W.A., and Mokady, O., Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning, Dev. Biol., 2006, vol. 298, pp. 368–378.

    Article  CAS  PubMed  Google Scholar 

  175. Polak, O., Loya, Y., Brickner, I., Kramarski-Winter, E., and Benayahu, Y., The widely-distributed indo-pacific zoanthid Palythoa tuberculosa: a sexually conservative strategist, Bull. Mar. Sci., 2011, vol. 87, no. 3, pp. 605–621.

    Article  Google Scholar 

  176. Polteva, D.G. and Aizenstadt, T.B., The fine structure of Obelia larvae (Hydrozoa). Interstitial cells differentiation at the early larval development, Tsitologiya, 1980, vol. 22, pp. 271–276.

    Google Scholar 

  177. Puente-Tapia, F.A., Garese, A., Delpiani, S.M., Acuña, F., and Genzano, G., Association between the parasitic larvae of the sea-anemone Peachia sp. (Cnidaria: Haloclavidae) and hydromedusae (Cnidaria: Hydrozoa) in the temperate southwestern Atlantic Ocean, Mar. Biodiversity, 2021, vol. 51, no. 5, p. 72.

    Article  Google Scholar 

  178. Pyataeva, S.V., Hopcroft, R.R., Lindsay, D.J., and Collins, A.G., Dna barcodes unite two problematic taxa: the meiobenthic Boreohydra simplex is a life-cycle stage of Plotocnide borealis (Hydrozoa: Aplanulata), Zootaxa, 2016, vol. 4150, no. 1, pp. 085–092.

  179. Quattrini, A.M., Rodriguez, E., Faircloth, B.C., et al., Paleoclimate ocean conditions shaped diversification of coral skeletal composition through deep time, Nat. Ecol. Evol., 2020, vol. 4, pp. 1531–1538.

    Article  PubMed  Google Scholar 

  180. Raff, R.A., Origins of the other metazoan body plans: the evolution of larval forms, Philos. Trans. R. Soc., B, 2008, vol. 363, no. 1496, pp. 1473–1479.

  181. Raikova, E.V., Life cycle, cytology, and morphology of Polypodium hydriforme, a coelenterate parasite of the eggs of acipenseriform fishes, J. Parasitol., 1994, vol. 80, no. 1, pp. 1–22.

    Article  CAS  PubMed  Google Scholar 

  182. Rakka, M., Godinho, A., Orejas, C., and Carreiro-Silva, M., Embryo and larval biology of the deep-sea octocoral Dentomuricea aff. meteor under different temperature regimes, PeerJ, 2021, vol. 9, p. e11604. https://doi.org/10.7717/peerj.11604

    Article  PubMed  PubMed Central  Google Scholar 

  183. Raskoff, K.A., Bathykorus bouilloni: a new genus and species of deep-sea jellyfish from the Arctic Ocean (Hydrozoa, Narcomedusae, Aeginidae), Zootaxa, 2010, vol. 2361, pp. 57–67.

    Article  Google Scholar 

  184. Rees, W.J., The development of the hydroid Corymorpha nutans M. Sars from the egg, J. Mar. Biol. Assoc. U. K., 1937, vol. 21, no. 2, pp. 743–746.

    Article  Google Scholar 

  185. Reitzel, A.M., Sullivan, J.C., and Finnerty, J.R., Qualitative shift to indirect development in the parasitic sea anemone Edwardsiella lineate, Integr. Comp. Biol., 2006, vol. 46, no. 6, pp. 827–837.

    Article  CAS  PubMed  Google Scholar 

  186. Reitzel, A.M., Burton, P.M., Krone, C., and Finnerty, J.R., Comparison of developmental trajectories in the starlet sea anemone Nematostella vectensis: embryogenesis, regeneration, and two forms of asexual fission, Invertebr. Biol., 2007, vol. 126, no. 2, pp. 99–112.

    Article  Google Scholar 

  187. Rentzsch, F., Fritzenwanker, J.H., Scholz, C.B., and Technau, U., FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis, Development, 2008, vol. 135, no. 10, pp. 1761–1769.

    Article  CAS  PubMed  Google Scholar 

  188. Riemann-Zürneck, K., Reproductive biology, oogenesis and early development in the brood-caring sea anemone Actinostola spetsbergensis (Anthozoa: Actiniaria), Helgol. Wiss. Meeresunters., 1976, vol. 28, no. 3, pp. 239–249.

    Article  Google Scholar 

  189. Riemann-Zürneck, K.A., How sessile are sea anemones? A review of free-living forms in the Actiniaria Cnidaria: Anthozoa, Mar. Ecol., 1998, vol. 19, no. 4, pp. 247–261.

    Article  Google Scholar 

  190. Riemann-Zürneck, K. and Iken, K., Corallimorphus profundus in shallow Antarctic habitats: bionomics, histology, and systematics (Cnidaria: Hexacorallia), Zool. Verh. Leiden, 2003, vol. 345, pp. 367–386.

    Google Scholar 

  191. Rinkevich, B. and Loya, Y., The reproduction of the red sea coral Stylophora pistillata. I. Gonads and planulae, Mar. Ecol. Prog. Ser., 1979, vol. 30, pp. 133–144.

    Article  Google Scholar 

  192. Rodriguez, E., Barbeitos, M.S., Brugler, M.R., et al., Hidden among sea anemones: the first comprehensive phylogenetic reconstruction of the order Actiniaria (Cnidaria, Anthozoa, Hexacorallia) reveals a novel group of hexacorals, PLoS One, 2014, vol. 9, no. 5, p. e96998.

    Article  PubMed  PubMed Central  Google Scholar 

  193. Ros-Rocher, N., Pérez-Posada, A., Leger, M.M., and Ruiz-Trillo, I., The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition, Open Biol., 2021, vol. 11, no. 2, p. 200359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Ruiz-Trillo, I. and de Mendoza, A., Towards understanding the origin of animal development, Development, 2020, vol. 147, no. 23, p. dev192575.

    Article  CAS  PubMed  Google Scholar 

  195. Ryland, J.S., Reproduction in Zoanthidea (Anthozoa: Hexacorallia), Invertebr. Reprod. Dev., 1997, vol. 31, nos. 1–3, pp. 177–188. https://doi.org/10.1080/07924259.1997.9672575

    Article  Google Scholar 

  196. Ryland, J.S., de Putron, S., Scheltema, R.S., Chimonides, P.J., and Zhadan, D.G., Semper’s (zoanthid) larvae: pelagic life, parentage and other problems, Hydrobiologia, 2000, vol. 440, pp. 191–198.

    Article  Google Scholar 

  197. Schiariti, A., Dutto, M.S., Morandini, A.C., et al., An overview of the Medusozoa from the Southwestern Atlantic, in Plankton Ecology of the Southwestern Atlantic: From the Subtropical to the Subantarctic Realm, 2018, pp. 413–449.

    Google Scholar 

  198. Schmich, J., Trepel, S., and Leitz, T., The role of GLWamides in metamorphosis of Hydractinia echinata, Dev. Genes Evol., 1998, vol. 208, pp. 267–273.

    Article  CAS  PubMed  Google Scholar 

  199. Schwarz, J.A., Krupp, D.A., and Weis, V.M., Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria, Biol. Bull., 1999, vol. 196, no. 1, pp. 70–79.

    Article  CAS  PubMed  Google Scholar 

  200. Schwarz, J., Weis, V., and Potts, D., Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantissima, Mar. Biol., 2002, vol. 140, no. 3, pp. 471–478.

    Article  Google Scholar 

  201. Scott, A. and Harrison, P.L., Embryonic and larval development of the host sea anemones Entacmaea quadricolor and Heteractis crispa, Biol. Bull., 2007, vol. 213, no. 2, pp. 110–121.

    Article  PubMed  Google Scholar 

  202. Sebe-Pedros, A. and Mendoza, A., Transcription factors and the origin of animal multicellularity, in Evolutionary Transitions to Multicellular Life, Ruiz-Trillo, I. and Nedelcu, A.M., Eds., Dordrecht: Springer, 2015, pp. 379–394.

    Google Scholar 

  203. Sebe-Pedros, A., Saudemont, B., and Chomsky, E., Cnidarian cell type diversity and regulation revealed by whole-organism single-cell RNA-Seq, Cell, 2018, vol. 173, no. 6, pp. 1520–1534.

    Article  CAS  PubMed  Google Scholar 

  204. Seipp, S., Wittig, K., Stiening, B., et al., Metamorphosis of Hydractinia echinata (Cnidaria) is caspase-dependent, Int. J. Dev. Biol., 2006, vol. 50, pp. 63–70.

    Article  CAS  PubMed  Google Scholar 

  205. Seipp, S., Schmich, J., Will, B., et al., Neuronal cell death during metamorphosis of Hydractina echinata (Cnidaria, Hydrozoa), Invertebr. Neurosci., 2010, vol. 10, no. 2, pp. 77–91.

    Article  CAS  Google Scholar 

  206. Shchelkanovtsev, Ya., Observations on the structure and development of Coelenterata, Izv. Obshch. Lyubit. Estestv., 1905, vol. 110, pp. 1–104.

    Google Scholar 

  207. Sherlock, R.E. and Robison, B.H., Effects of temperature on the development and survival of Nanomia bijuga (Hydrozoa, Siphonophora), Invertebr. Biol., 2000, vol. 119, no. 4, pp. 379–385.

    Article  Google Scholar 

  208. Siebert, A.E. and Spaulding, J.G., The taxonomy, development and brooding behavior of the anemone, Cribrinopsis fernaldi sp. nov., Biol. Bull., 1976, vol. 150, no. 1, pp. 128–138.

    Article  Google Scholar 

  209. Sinigaglia, C., Busengdal, H., Lerner, A., Oliveri, P., and Rentzsch, F., Molecular characterization of the apical organ of the anthozoan Nematostella vectensis, Dev. Biol., 2015, vol. 398, no. 1, pp. 120–133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Sommer, C., Post-embryonic larval development and metamorphosis of the hydroid Eudendrium racemosum (Cavolini) (Hydrozoa, Cnidaria), Helgol. Wiss. Meeresunters., 1990, vol. 44, no. 3, pp. 425–444.

    Article  Google Scholar 

  211. Sommer, C., Larval biology and dispersal of Eudendrium racemosum (Hydrozoa, Eudendriidae), Sci. Mar., 1992, vol. 56, no. 2, pp. 205–211.

    Google Scholar 

  212. Spaulding, J.G., Embryonic and larval development in sea anemones (Anthozoa: Actiniaria), Am. Zool., 1974, vol. 14, pp. 511–520.

    Article  Google Scholar 

  213. Spindler, K.D. and Müller, W.A., Induction of metamorphosis by bacteria and by a lithium-pulse in the larvae of Hydractinia echinata (Hydrozoa), Wilhelm Roux’ Arch. Entwicklungsmech. Org., 1972, vol. 169, pp. 271–280.

    Article  Google Scholar 

  214. Stampar, S.N., Maronna, M.M., Kitahara, M.V., Reimer, J.D., and Morandini, A.C., Fast-evolving mitochondrial DNA in Ceriantharia: a reflection of Hexacorallia paraphyly?, PLoS One, 2014, vol. 9, no. 1, p. e86612.

    Article  PubMed  PubMed Central  Google Scholar 

  215. Stampar, S.N., Morandini, A.C., Branco, L.C., Da Silveira, F.L., and Migotto, A.E., Drifting in the oceans: Isarachnanthus nocturnus (Cnidaria, Ceriantharia, Arachnactidae), an anthozoan with an extended planktonic stage, Mar. Biol., 2015, vol. 162, no. 11, pp. 2161–2169.

    Article  Google Scholar 

  216. Stampar, S.N., Broe, M.B., Macrander, J., Reitzel, A.M., Brugler, M.R., and Daly, M., Linear mitochondrial genome in Anthozoa (Cnidaria): a case study in Ceriantharia, Sci. Rep., 2019, vol. 9, no. 1, p. 6094.

    Article  PubMed  PubMed Central  Google Scholar 

  217. Stefanik, D.J., Lubinski, T.J., Granger, B.R., et al., Production of a reference transcriptome and transcriptomic database (EdwardsiellaBase) for the lined sea anemone, Edwardsiella lineata, a parasitic cnidarian, BMC Genomics, 2014, vol. 15, pp. 1–20.

    Article  Google Scholar 

  218. Steinmetz, P.R., Kraus, J.E., and Larroux, C., Independent evolution of striated muscles in cnidarians and bilaterians, Nature, 2012, vol. 487, no. 7406, pp. 231–234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  219. Steinmetz, P.R., Aman, A., Kraus, J.E., and Technau, U., Gut-like ectodermal tissue in a sea anemone challenges germ layer homology, Nat. Ecol. Evol., 2017, vol. 1, no. 10, pp. 1535–1542.

    Article  PubMed  PubMed Central  Google Scholar 

  220. Straehler-Pohl, I. and Jarms, G., Life cycle of Carybdea marsupialis Linnaeus, 1758 (Cubozoa, Carybdeidae) reveals metamorphosis to be a modified strobilation, Mar. Biol., 2005, vol. 147, no. 6, pp. 1271–1277.

    Article  Google Scholar 

  221. Stricker, S.A., An ultrastructural study of larval settlement in the sea anemone Urticina crassicornis (Cnidaria, Actiniaria), J. Morphol., 1985, vol. 186, no. 2, pp. 237–253.

    Article  Google Scholar 

  222. Stumpf, M., Will, B., Wittig, K., Kasper, J., Fischer, B., Schmich, J., Seipp, S., and Leitz, T., An organizing region in metamorphosing hydrozoan planula larvae—stimulation of axis formation in both larval and in adult tissue, Int. J. Dev. Biol., 2010, vol. 54, pp. 795–802.

    Article  CAS  PubMed  Google Scholar 

  223. Sun, Z., Hamel, J.F., and Mercier, A., Planulation of deep-sea octocorals in the NW Atlantic, Coral Reefs, 2009, vol. 28, no. 3, p. 781.

    Article  Google Scholar 

  224. Sun, Z., Hamel, J.F., and Mercier, A., Planulation, larval biology, and early growth of the deep-sea soft corals Gersemia fruticosa and Duva florida (Octocorallia: Alcyonacea), Invertebr. Biol., 2011, vol. 130, no. 2, pp. 91–99.

    Article  Google Scholar 

  225. Suzuki, H., Notes on Cornularia (Stolonifera, Alcyonaria) found in the vicinity of the manazuru marine biological laboratory, Yokohama Natl. Univ. Sci. Bull., Cat. 2: Biol. Earth Sci., 1971, vol. 18, pp. 1–6. https://ynu.repo.nii.ac.jp/records/1601.

    Google Scholar 

  226. Szmant-Froelich, A., Yevich, P., and Pilson, M.E., Gametogenesis and early development of the temperate coral Astrangia danae (Anthozoa: Scleractinia), Biol. Bull., 1980, vol. 158, no. 2, pp. 257–269.

    Article  Google Scholar 

  227. Thomas, M.B. and Edwards, N.C., Cnidaria: hydrozoa, in Microscopic Anatomy of Invertebrates, Harrison, F.W. and Westfall, J.A., Eds., New York: Wiley-Liss, 1991, vol. 2, рр. 91–183.

    Google Scholar 

  228. Thomas, M.B., Freeman, G., and Martin, V.J., The embryonic origin of neurosensory cells and the role of nerve cells in metamorphosis in Phialidium gregarium (Cnidaria, Hydrozoa), Int. J. Invertebr. Reprod. Dev., 1987, vol. 11, no. 3, pp. 265–285.

    Article  Google Scholar 

  229. Tonra, K.J., Wells, C.D., and Lasker, H.R., Spawning, embryogenesis, settlement, and post-settlement development of the gorgonian Plexaura homomalla, Invertebr. Biol., 2021, vol. 140, no. 2, p. e12319.

    Article  Google Scholar 

  230. Toshino, S., Miyake, H., Ohtsuka, S., et al., Development and polyp formation of the giant box jellyfish Morbakka virulenta (Kishinouye, 1910) (Cnidaria: Cubozoa) collected from the Seto Inland Sea, western Japan, Plankton Benthos Res., 2013, vol. 8, no. 1, pp. 1–8.

    Article  Google Scholar 

  231. Toshino, S., Miyake, H., and Iwanaga, S., Development of Copula sivickisi (Stiasny, 1926) (Cnidaria: Cubozoa: Carybdeidae: Tripedaliidae) collected from the Ryukyu Archipelago, southern Japan, Plankton Benthos Res., 2014, vol. 9, no. 1, pp. 32–41.

    Article  Google Scholar 

  232. Toshino, S., Miyake, H., Ohtsuka, S., et al., Monodisc strobilation in Japanese giant box jellyfish Morbakka virulenta (Kishinouye, 1910): a strong implication of phylogenetic similarity between Cubozoa and Scyphozoa, Evol. Dev., 2015, vol. 17, no. 4, pp. 231–239.

    Article  PubMed  Google Scholar 

  233. Toshino, S., Miyake, H., and Shibata, H., Development of Carybdea brevipedalia Kishinouye, 1891 (Cnidaria: Cubozoa: Carybdeida: Carybdeidae) collected from northern Japan, Plankton Benthos Res., 2018, vol. 13, no. 3, pp. 116–128.

    Article  Google Scholar 

  234. Tranter, P.R., Nicholson, D.N., and Kinchington, D., A description of spawning and post-gastrula development of the cool temperate coral, Caryophyllia smithi, J. Mar. Biol. Assoc. U. K., 1982, vol. 62, no. 4, pp. 845–854.

    Article  Google Scholar 

  235. Vandermeulen, J.H., Studies on reef corals. II. Fine structure of planktonic planula larva of Pocillopora damicornis, with emphasis on the aboral epidermis, Mar. Biol., 1974, vol. 27, pp. 239–249.

    Article  Google Scholar 

  236. Vetrova, A.A., Lebedeva, T.S., Saidova, A.A., Kupaeva, D.M., Kraus, Y.A., and Kremnyov, S.V., From apolar gastrula to polarized larva: embryonic development of a marine hydroid, Dynamena pumila, Dev. Dyn., 2022, vol. 251, no. 5, pp. 795–825.

    Article  CAS  PubMed  Google Scholar 

  237. Vetrova, A.A., Kupaeva, D.M., Kizenko, A., Lebedeva, T.S., Walentek, P., Tsikolia, N., and Kremnyov, S.V., The evolutionary history of Brachyury genes in Hydrozoa involves duplications, divergence, and neofunctionalization, Sci. Rep., 2023, vol. 13, no. 1, p. 9382.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  238. van de Vyver, G., A comparative study of the embryonic development of hydrozoa athecata, in Developmental and Cellular Biology of Coelenterates, Tardent, P. and Tardent, R., Eds., Amsterdam: Elsevier, 1980, pp. 109–120.

    Google Scholar 

  239. Wang, J., Zhang, L., Lian, S., et al., Evolutionary transcriptomics of metazoan biphasic life cycle supports a single intercalation origin of metazoan larvae, Nat. Ecol. Evol., 2020, vol. 4, no. 5, pp. 725–736.

    Article  PubMed  Google Scholar 

  240. Weinberg, S. and Weinberg, F., The life cycle of a gorgonian: Eunicella singularis (Esper, 1794), Bijdragen Dierkunde, 1979, vol. 48, no. 2, pp. 127–140.

    Article  Google Scholar 

  241. Weis, V.M., Keene, D.R., and Buss, L.W., Biology of Hydractiniid hydroids. 4. Ultrastructure of the planula of Hydractinia echinata, Biol. Bull., 1985, vol. 168, no. 3, pp. 403–418.

    Article  Google Scholar 

  242. Werner, B., Polypengeneration und Entwicklungsgeschichte von Eucheilota maculata (Thecata-Leptomedusae) Mit einem Beitrag zur Methodik der Kultur mariner Hydroiden, Helgol. Wiss. Meeresunters., 1968, vol. 18, pp. 136–168.

    Article  Google Scholar 

  243. Werner, B., Cutress, C.E., and Studebaker, J.P., Life cycle of Tripedalia cystophora Conant (Cubomedusae), Nature, 1971, vol. 232, no. 5312, pp. 582–583.

    Article  CAS  PubMed  Google Scholar 

  244. Widersten, B., Genital organs and fertilization in some Scyphozoa, Zool. Bidrag. Upps., 1965, vol. 37, pp. 45–57.

    Google Scholar 

  245. Widersten, B., On the morphology of actiniarian larvae, Zool. Scr., 1974, vol. 2, no. 4, pp. 119–124.

    Article  Google Scholar 

  246. Widmer, C.L., Life cycle of Chrysaora fuscescens (Cnidaria: Scyphozoa) and a Key to sympatric ephyrae 1, Pac. Sci., 2008, vol. 62, no. 1, pp. 71–82.

    Article  Google Scholar 

  247. Wietrzykowski, W., Sur le développement des Lucernaridés (note préliminaire), Arch. Zool. Exp., 1910, vol. 5, pp. 10–27.

    Google Scholar 

  248. Wietrzykowski, W., Recherches sur le development des Lucernaires, Arch. Zool. Exp. Gen., Ser. 5, 1912, vol. 10, pp. 1–95.

    Google Scholar 

  249. Wilson, E.B., The development of Renilla, Philos. Trans. R. Soc. London, 1883, vol. 174, pp. 723–815.

    Article  Google Scholar 

  250. Wittig, K., Kasper, J., Seipp, S., and Leitz, T., Evidence for an instructive role of apoptosis during the metamorphosis of Hydractinia echinata (Hydrozoa), Zoology, 2011, vol. 114, no. 1, pp. 11–22.

    Article  PubMed  Google Scholar 

  251. Wolfowicz, I., Baumgarten, S., Voss, P.A., et al., Aiptasia sp. larvae as a model to reveal mechanisms of symbiont selection in cnidarians, Sci. Rep., 2016, vol. 6, no. 1, pp. 1–12.

    Article  Google Scholar 

  252. WoRMS—World Register of Marine Species. www.marinespecies.org/.

  253. Wulfert, J., Die Embryonalyentwicklung von Gonothyraea loveni Allm, Zeitschrifts Wiss. Zool., 1902, vol. 71, pp. 296–325.

    Google Scholar 

  254. Yamashita, K., Kawaii, S., Nakai, M., and Fusetani, N., Larval behavioral, morphological changes, and nematocyte dynamics during settlement of actinulae of Tubularia mesembryanthemum, Allman 1871 (Hydrozoa: Tubulariidae), Biol. Bull., 2003, vol. 204, no. 3, pp. 256–269.

    Article  PubMed  Google Scholar 

  255. Ying, H., Cooke, I., Sprungala, S., et al., Comparative genomics reveals the distinct evolutionary trajectories of the robust and complex coral lineages, Genome Biol., 2018, vol. 19, no. 175. https://doi.org/10.1186/s13059-018-1552-8

  256. Yuan, D., Nakanishi, N., Jacobs, D.K., and Hartenstein, V., Embryonic development and metamorphosis of the scyphozoan Aurelia, Dev. Genes Evol., 2008, vol. 218, no. 10, pp. 525–539.

    Article  PubMed  Google Scholar 

  257. Zakhvatkin, A.A., Sravnitel’naya embriologiya nizshikh bespozvonochnykh (Comparative Embryology of Lower Invertebrates), Moscow: Nauka, 1949.

  258. Zalenskij, W., Solmundella und actinula, Mem. Acad. Sci. St.-Petersbourg, 1911, vol. 30, no. 6, pp. 1–70.

  259. Zapata, F., Goetz, F.E., Smith, S.A., et al., Phylogenomic analyses support traditional relationships within Cnidaria, PLoS One, 2015, vol. 10, no. 10, p. e0139068.

    Article  PubMed  PubMed Central  Google Scholar 

  260. Zaslow, R.B. and Benayahu, Y., Longevity, competence and energetic content in planulae of the soft coral Heteroxenia fuscescens, J. Exp. Mar. Biol. Ecol., 1996, vol. 206, nos. 1–2, pp. 55–68.

    Article  Google Scholar 

Download references

ACKNOWLEDGMENTS

I would like to thank my colleagues Igor Kosevich, Tatiana Mayorova, Grigory Genikhovich, Boris Osadchenko, Lucas Leclere, Catriona Munro, Elena Dmitrieva, Evelyn Houliston, Stanislav Kremnyov, and Aleksandra Vetrova for their collaboration and fruitful discussions. I am very grateful to the staff of the Shared Research Facility “Electron microscopy in life sciences” of Moscow State University for their help and support.

Funding

This work was supported by the Russian Science Foundation research project (grant no. 22-24-01166).

Author information

Authors and Affiliations

  1. Faculty of Biology, Moscow State University, 119934, Moscow, Russia

    Y. A. Kraus

  2. Koltzov Institute of Developmental Biology of the Russian Academy of Sciences, 119334, Moscow, Russia

    Y. A. Kraus

Authors
  1. Y. A. Kraus
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y. A. Kraus.

Ethics declarations

CONFLICT OF INTEREST

As author of this work, I declare that I have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The data from papers published in 2023 were added to the review in December 2023 by permission of the journal editorial board.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kraus, Y.A. Cnidarian Larvae: True Planulae, Other-Than-Planulae, and Planulae That Don’t Look Like Planulae. Russ J Dev Biol 54 (Suppl 1), S23–S61 (2023). https://doi.org/10.1134/S1062360423070044

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360423070044

Keywords:

Search

Navigation