Russian Journal of Marine Biology

, Volume 42, Issue 2, pp 128–138

An original description of the larval stages of Phoronis australis Haswell, 1883 and an analysis of the world fauna of phoronid larvae

  • E. N. Temereva
  • T. V. Neretina
  • A. N. Stupnikova
Invertebrate Zoology

Abstract

Phoronida is a phylum of marine invertebrates; they have a worldwide distribution and form huge benthic aggregations in some areas. The taxonomy of Phoronida remains very poorly developed; only 13 species of phoronids have been described worldwide, while approximately 40 varieties of competent larvae are known. Morphological description of phoronid larvae and the search for correspondence between the larval and adult forms make an important contribution to the taxonomy of this enigmatic group. We present an original description of the larval forms of Phoronis australis Haswell, 1883. The larvae and adults of P. australis were collected in the plankton of Nha Trang Bay in the South China Sea. For the first time, the external morphology of larval forms of P. australis was described at the stages of 4, 8, and 20 tentacles. The basic distinguishing features of Phoronis australis larvae were determined: opaque integuments, the presence of a characteristic dark pigmentation of the oral field epidermis, of the unpaired ventral stomach diverticulum, and more than 20 tentacles in the competent larvae. A molecular-genetic analysis based on comparison of the DNA sequences of the 18S rDNA and 28S rDNA nuclear genes confirmed the identity of the phoronid larvae that were found in the planktonic samples from Nhatrang Bay and adult P. australis that were collected in the same area. The problems of Phoronida taxonomy and correspondence of larval and adult forms can be solved only with a complex approach that involves both morphological and molecular-genetic information.

Keywords

Phoronida taxonomy 18S 28S morphology larvae 

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References

  1. 1.
    Vyshkvartsev, D.I., Lebedev, E.B., and Kalashnikov, V.Z., Sequences of the typhoon “Vera”: invertebrates washed on a sand spit in Possjet Bay, Sea of Japan, Biol. Morya (Vladivostok, Russ. Fed.), 1990, no. 5, pp. 78–80.Google Scholar
  2. 2.
    Malakhov, V.V. and Temereva, E.N., Embryonic development of the phoronid Phoronis ijimai, Russ. J. Mar. Biol., 2000, vol. 26, no. 6, pp. 412–421.CrossRefGoogle Scholar
  3. 3.
    Omelyanenko, V.A. and Kulikova, V.A., Pelagic larvae of benthic invertebrates of the Vostok Bay, Peter the Great Bay, Sea of Japan: composition, phenology, and population dynamics, Russ. J. Mar. Biol., 2011, vol. 37, no. 1, pp. 7–22.Google Scholar
  4. 4.
    Temereva, E.N., New species Phoronopsis malakhovi (Lophophorata, Phoronida) from the South-China Sea, Zool. Zh., 2000, vol. 79, no. 9, pp. 1088–1093.Google Scholar
  5. 5.
    Temereva, E.N. and Malakhov, V.V., New species of drilling phoronids Phoronis svetlanae (Lophophorata, Phoronida) from the Sea of Japan, Zool. Zh., 1999, vol. 78, no. 5, pp. 626–630.Google Scholar
  6. 6.
    Temereva, E.N. and Malakhov, V.V., A key to the identification of phoronid larvae (Phoronida, Lophophorata) from the Sea of Japan, Zool. Zh., 2004, vol. 83, no. 9, pp. 1115–1126.Google Scholar
  7. 7.
    Temereva, E.N. and Malakhov, V.V., On the organization of the lophophore in phoronids (Lophophorata: Phoronida), Russ. J. Mar. Biol., 2009, vol. 35, no. 6, pp. 479–489.CrossRefGoogle Scholar
  8. 8.
    Temereva, E.N., Malakhov V.V., and Chernyshev, A.V., Giant actinotroch, a larva of Phoronida from the South China Sea: the giant larva phenomenon, Dokl. Akad. Nauk, 2006, vol. 410, no. 5, pp. 410–413.Google Scholar
  9. 9.
    Temereva, E.N., Malakhov, V.V., Yakovis, E.L., and Fokin, M.V., Phoronis ovalis (Phoronida, Lophophorata) in the White Sea: the first finding of phoronids in the Arctic Basin, Dokl. Akad. Nauk, 2000, vol. 374, no. 4, pp. 571–573.Google Scholar
  10. 10.
    Álvarez, F., Emig, C.C., Roldán, C., and Viéitez, J.M., Lophophorata: Phoronida, Brachiopoda, Fauna Ibérica, Madrid: Museo de Ciencias Naturales, CSIC, 2005, vol. 27.Google Scholar
  11. 11.
    Emig, C.C., Remarques sur la systématique des Phoronidiens. X. Note sur l’écologie, la morphologie et la taxonomie de Phoronis ijimai et Phoronis vancouverensis, Mar. Biol., 1971, vol. 8, pp. 154–159.CrossRefGoogle Scholar
  12. 12.
    Emig, C.C., Taxonomie et systématique des Phoronidiens, Bull. Mus. Nat. Hist. Nat. Paris, 3e Sér.: Zool., 1971, vol. 8, pp. 469–568.Google Scholar
  13. 13.
    Emig, C.C., Notes sur la localisation, l’écologie et la taxonomie des Phoronidiens, Téthys, 1977, vol. 7, no. 4, pp. 357–364.Google Scholar
  14. 14.
    Emig, C.C., British and other phoronids, Synop. Br. Fauna, 1979, vol. 13, pp. 1–57.Google Scholar
  15. 15.
    Emig, C.C., The biology of Phoronida, Adv. Mar. Biol., 1982, vol. 19, pp. 2–90.Google Scholar
  16. 16.
    Emig, C.C., Phylogenetic systematics in Phoronida (Lophophorata), Z. Zool. Syst. Evol.-Forsch., 1985, vol. 23, no. 3, pp. 184–193.CrossRefGoogle Scholar
  17. 17.
    Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap, Evolution, 1985, vol. 39, pp. 783–791.CrossRefGoogle Scholar
  18. 18.
    Forneris, L., Phoronidea from Brazil, Bol. Inst. Océanogr. Sao Paulo, 1959, vol. 10, no. 2, pp. 1–105.Google Scholar
  19. 19.
    Garlitskaya, L., Neretina, T., Schepetov, D., et al., Cryptic diversity of the “cosmopolitan” harpacticoid copepod Nannopus palustris: genetic and morphological evidence, Mol. Ecol., 2012, vol. 21, pp. 5336–5347.CrossRefGoogle Scholar
  20. 20.
    Giribet, G., Carranza, S., Baguñà, J., et al., First molecular evidence for the existence of a Tardigrada + Arthropoda clade, Mol. Biol. Evol., 1996, vol. 13, pp. 76–84.CrossRefPubMedGoogle Scholar
  21. 21.
    Hirose, M., Fukiage, R., Katoh, T., and Kajihara, H., Description and molecular phylogeny of a new species of Phoronis (Phoronida) from Japan, with a redescription of topotypes of P. ijimai Oka, 1897, ZooKeys, 2014, vol. 398, pp. 1–31.CrossRefPubMedGoogle Scholar
  22. 22.
    Ikeda, I., Observation on the development, structure and metamorphosis of Actinotrocha, J. Coll. Sci. Imp. Univ. Tokyo, 1901, vol. 13, pp. 507–591.Google Scholar
  23. 23.
    Johnson, K.B, Phoronida, An Identification Guide to the Larval Marine Invertebrates of the Pacific Northwest, Corvallis: Oregon State Univ. Press, 2001), pp. 251–257.Google Scholar
  24. 24.
    Johnson, K.B. and Zimmer, R.L., Phylum Phoronida, in Atlas of Marine Invertebrate Larvae, San Diego: Academic, 2002), pp. 429–439.Google Scholar
  25. 25.
    Littlewood, D.T., Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences, Mol. Phylogenet. Evol., 1994, vol. 3, pp. 221–229.CrossRefPubMedGoogle Scholar
  26. 26.
    Saitou, N. and Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 1987, vol. 4, pp. 406–425.PubMedGoogle Scholar
  27. 27.
    Santagata, S. and Cohen, B.L., Phoronid phylogenetics (Brachiopoda; Phoronata): evidence from morphological cladistics, small and large subunit rDNA sequences, and mitochondrial cox1, Zool. J. Linn. Soc., 2009, vol. 157, pp. 34–50.Google Scholar
  28. 28.
    Santagata, S. and Zimmer, R.L., Comparison of the neuromuscular system among actinotroch larvae: systematic and evolutionary implications, Evol. Devel., 2002, vol. 4, pp. 43–54.CrossRefGoogle Scholar
  29. 29.
    Selys-Longchamps, M., Phoronis, Fauna und Flora des Golfes von Neapel, 1907), vol. 30.Google Scholar
  30. 30.
    Silen, L., Developmental biology of Phoronidea of the Gullmar Fiord area (west coast of Sweden), Acta Zool. (Stockholm), 1954, vol. 35, pp. 215–257.CrossRefGoogle Scholar
  31. 31.
    Tamura, K. and Nei, M., Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees, Mol. Biol. Evol., 1993, vol. 10, pp. 512–526.PubMedGoogle Scholar
  32. 32.
    Tamura, Y., Busby, C., and Blum, P., Izu-Bonin-Mariana Rear Arc: the missing half of the subduction factory, IODP Sci. Prosp., 2013.Google Scholar
  33. 33.
    Temereva, E.N., New data on distribution, morphology and taxonomy of phoronid larvae (Phoronida, Lophophorata), Invertebr. Zool., 2009, vol. 6, no. 1, pp. 47–64.Google Scholar
  34. 34.
    Temereva, E.N., Organization of the coelomic system in Phoronis australis (Lophotrochozoa: Phoronida) and consideration of the coelom in the lophophorates, J. Zool., 2015, vol. 296, no. 2, pp. 79–94.CrossRefGoogle Scholar
  35. 35.
    Temereva, E.N. and Neretina, T.V., A distinct phoronid larva: morphological and molecular evidence, Invertebr. Syst., 2013, vol. 27, no. 6, pp. 622–633.Google Scholar
  36. 36.
    Thompson, J.D., Higgins, D.G., and Gibson, T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res., 1994, vol. 22, pp. 4673–4680.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Whiting, M.F., Carpenter, J.M., Wheeler, Q.D., and Wheeler, W.C., The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology, Syst. Biol., 1997, vol. 46, pp. 1–68.PubMedGoogle Scholar
  38. 38.
    Wright, S., Description of two tubicolar animals, Edinburgh New Phil. J., 1856, vol. 4, pp. 3–13.Google Scholar
  39. 39.
    Zimmer, R.L., Reproductive biology and development of Phoronida: PhD Thesis, Univ. of California, 1964).Google Scholar
  40. 40.
    Zimmer, R.L., The comparative structure of the preoral hood coelom in Phoronida and the fate of this cavity during and after metamorphosis, in Settlement and Metamorphosis of Marine Invertebrate Larvae, New York: Elsevier, 1978), pp. 23–40.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • E. N. Temereva
    • 1
  • T. V. Neretina
    • 2
  • A. N. Stupnikova
    • 3
  1. 1.Department of BiologyMoscow State UniversityMoscowRussia
  2. 2.White Sea Biological StationMoscow State UniversityMoscowRussia
  3. 3.Shirshov Institute of OceanologyRussian Academy of SciencesMoscowRussia

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