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Genetic identity of two physonect siphonophores from Southern Ocean waters – the enigmatic taxon Mica micula and Pyrostephos vanhoeffeni

Published online by Cambridge University Press:  15 April 2018

Anna Panasiuk ,
Anna Jażdżewska ,
Angelika Słomska ,
Marta Irzycka  and
Justyna Wawrzynek
Anna Panasiuk*
Affiliation:
Department of Marine Plankton Research, University of Gdansk, Faculty of Oceanography and Geography, Institute of Oceanography, Av. J.M. Piłsudskiego 46, 81-378 Gdynia, Poland
Anna Jażdżewska
Affiliation:
Department of Invertebrate Zoology and Hydrobiology, University of Lodz, Faculty of Biology and Environmental Protection, 12/16 Banacha St., 90-237 Łódź, Poland
Angelika Słomska
Affiliation:
Department of Marine Plankton Research, University of Gdansk, Faculty of Oceanography and Geography, Institute of Oceanography, Av. J.M. Piłsudskiego 46, 81-378 Gdynia, Poland
Marta Irzycka
Affiliation:
Department of Invertebrate Zoology and Hydrobiology, University of Lodz, Faculty of Biology and Environmental Protection, 12/16 Banacha St., 90-237 Łódź, Poland
Justyna Wawrzynek
Affiliation:
Department of Marine Plankton Research, University of Gdansk, Faculty of Oceanography and Geography, Institute of Oceanography, Av. J.M. Piłsudskiego 46, 81-378 Gdynia, Poland
*
Correspondence should be addressed to: Anna Panasiuk, Department of Marine Plankton Research, University of Gdansk, Faculty of Oceanography and Geography, Institute of Oceanography, Av. J.M. Piłsudskiego 46, 81-378 Gdynia, Poland email: [email protected]
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Abstract

Based on some coincident morphological characters and distribution, it was believed for a long time that Mica micula was the post-larval stage of a species of Bargmannia, a genus having a very wide geographic distribution. Recent studies, however, have shown that it is much more likely to be the post-larval form of the physonect Pyrostephos vanhoeffeni, which is very common in both Antarctic and sub-Antarctic waters. Until now, molecular evidence to support this theory has been lacking. In the present study 34 nectophores of P. vanhoeffeni and four colonies of M. micula collected from three areas in the Southern Ocean were analysed for the 16S rRNA gene. Five haplotypes were identified, which formed two clearly distinct lineages. Three haplotypes were found exclusively in Admiralty Bay and were shared between individuals of both studied taxa, confirming that M. micula is indeed the post-larval stage of P. vanhoeffeni. Two additional haplotypes were found in one open ocean locality and in Admiralty Bay.

Keywords

Siphonophora (Pyrostephos vanhoeffeni, Mica micula)Southern Oceangenetic identity
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 2 , March 2019 , pp. 303 - 310
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

REFERENCES

Alvarino, A. (1963) Chaetognatha, Siphonophorae, and Medusae in the Gulf of Siam and the South China Sea. (Outline of the studies that have been made). Report on the results of the NAGA Expedition. Southeast Asia Research Project. San Diego, CA: Scripps Institution of Oceanography, pp. 104–108.Google Scholar
Alvarino, A. (1971) Siphonophores of the Pacific with a review of the world distribution. San Diego, CA: Scripps Institution of Oceanography. https://escholarship.org/uc/item/6zm3c9zb.Google Scholar
Alvarino, A., Wojtan, J.M. and Martinez, M.R. (1990) Antarctic Siphonophores from plankton samples of the United States Antarctic Research Program. Antarctic Research Series 49, 1–436.Google Scholar
Boero, F., Bouillon, J., Gravili, C., Miglietta, M.P., Parsons, T. and Piraino, S. (2008) Gelatinous plankton: irregularities rule the world (sometimes). Marine Ecology Progress Series 356, 299–310.Google Scholar
Bucklin, A., Ortman, B.D., Jennings, R.M., Nigro, L.M., Sweetman, C.J., Copley, N.J., Sutton, T. and Wiebe, P.H. (2010) A “Rosetta Stone” for metazoan zooplankton: DNA barcode analysis of species diversity of the Sargasso Sea (Northwest Atlantic Ocean). Deep Sea Research Part II 57, 2234–2247.Google Scholar
Cunningham, C. and Buss, W. (1993) Molecular evidence for multiple episodes of paedomorphosis in the family Hydractiniidae. Biochemical Systematics and Ecology 21, 57–69.Google Scholar
Dunn, C.W. (2005) Complex colony-level organization of the deep-sea siphonophore Bargmannia elongata (Cnidaria, Hydrozoa) is directionally asymmetric and arises by the subdivision of pro-buds. Developmental Dynamics 234, 835–845.Google Scholar
Dunn, C.W. (2009) Siphonophores. Current Biology 19, 233–234.Google Scholar
Dunn, C.W., Pugh, P.R. and Haddock, S.H.D. (2005) Molecular phylogenetics of the Siphonophora (Cnidaria), with implications for the evolution of functional specialisation. Systematic Biology 54, 916–935.Google Scholar
Folmer, O., Black, M., Hoen, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Fuentes, V., Schnack-Shiel, S.B., Schloss, I.R. and Esnal, G.G. (2008) Mesozooplankton of Potter Cove: community composition and seasonal distribution in 2002 and 2003. Berichte zur Polar-und Meeresforschung 571, 75–84.Google Scholar
GBIF (Global Biodiversity Information Facility) data portal: http://www.gbif.org/species/2264856 (Bargmannia elongata); accessed via GBIF.org on 2.8.2017.Google Scholar
Geller, J., Meyer, C., Parker, M. and Hawk, H. (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources 13, 851–861.Google Scholar
Grossmann, M.M., Lindsay, D.J. and Collins, A.G. (2013a) The end of an enigmatic taxon: Eudoxia macra is the eudoxid stage of Lensia cossack (Siphonophora, Cnidaria). Systematics and Biodiversity 11, 381–387.Google Scholar
Grossmann, M.M., Lindsay, D.J. and Fuentes, V. (2013b) A redescription of the post-larval physonect siphonophore stage known as Mica micula Margulis 1982, from Antarctica, with notes on its distribution and identity. Marine Ecology 34, 63–70.Google Scholar
Grossmann, M.M., Nishikawa, J. and Lindsay, D.J. (2015) Diversity and community structure of pelagic cnidarians in the Celebes and Sulu Seas, southeast Asian tropical marginal seas. Deep Sea Research Part I 100, 54–63.Google Scholar
Guerrero, E., Gili, J.-M., Rodriguez, C., Araujo, E.M., Canepa, A., Calbet, A., Genzano, G., Mianzan, H.W. and Gonzalez, R.A. (2013) Biodiversity and distribution patterns of planktonic cnidarians in San Matías Gulf, Patagonia, Argentina. Marine Ecology 34, 71–82.Google Scholar
Hardy, A.C. and Gunther, E.R. (1935) The plankton of the South Georgia whaling grounds and adjacent waters, 1926–1927. Discovery Reports 11, 1–456.Google Scholar
Hebert, P.D.N., Ratsingham, S. and de Waard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit I divergences among closely related species. Proceedings of the Royal Society B, Biological Sciences 270, 96–99.Google Scholar
Heimeier, D., Lavery, S. and Sewell, M.A. (2010) Using DNA barcoding and phylogenetics to identify Antarctic invertebrate larvae: lessons from a large scale study. Marine Genomics 3, 165–177.Google Scholar
Hillis, D.M., Mable, B.K. and Moritz, C. (1996) Applications of molecular systematics. In Hillis, D.M., Moritz, C. and Mable, B. (eds) Molecular systematics. Sunderland, MA: Sinauer Associates, pp. 515–543.Google Scholar
Hoareau, T.B. and Boissin, E. (2010) Design of phylum-specific hybrid primers for DNA barcoding: addressing the need for efficient COI amplification in the Echinodermata. Molecular Ecology Resources 10, 960–967.Google Scholar
Hosia, A., Stemmann, L. and Youngbluth, M. (2008) Distribution of net-collected planktonic cnidarians along the northern Mid-Atlantic Ridge and their associations with the main water masses. Deep Sea Research Part II 55, 106–118.Google Scholar
Jinbo, U., Kato, T. and Ito, M. (2011) Current progress in DNA barcoding and future implications for entomology. Entomological Science 14, 107–124.Google Scholar
Katoh, K., Misawa, K., Kuma, K. and Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.Google Scholar
Kirkpatrick, P.A. and Pugh, P.R. (1984) Siphonophores and velellids. Linnean Society Synopses of the British Fauna (New Series) 29, 1–154.Google Scholar
Kumar, S., Stecher, G. and Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Laakmann, S. and Holst, S. (2014) Emphasizing the diversity of North Sea hydromedusae by combined morphological and molecular methods. Journal of Plankton Research 36, 64–76.Google Scholar
Lindsay, D. (2006) A checklist of midwater cnidarians and ctenophores from Sagami Bay species sampled during submersible surveys from 1993–2004. Bulletin of the Plankton Society of Japan 53, 104–110.Google Scholar
Lindsay, D. and Hunt, J.C. (2005) Biodiversity in midwater cnidarians and ctenophores: submersible-based results from deep-water bays in the Japan Sea and north-western Pacific. Journal of the Marine Biological Association of the United Kingdom 85, 503–517.Google Scholar
Lindsay, D., Guerrero, E., Grossmann, M. and Fuentes, V. (2014) Southern ocean gelatinous zooplankton. In De Broyer, C., Koubi, P., Griffiths, H., Raymond, B., d'Udekem d'Acoz, C., Van de Putte, A., Danis, B., David, B., Grant, S., Gutt, J., Held, C., Hosie, G., Huettmann, F., Post, A. and Ropert-Coudert, Y. (eds.) Biogeographic atlas of the Southern Ocean. Cambridge: Scientific Committee on Antarctic Research, pp. 266–275.Google Scholar
Lindsay, D., Umetsu, M., Grossmann, M., Miyake, H. and Yamamoto, H. (2015a) The gelatinous macroplankton community at the Hatoma Knoll hydrothermal vent. In Ishibashi, J., Okino, K. and Sunamura, M. (eds) Subseafloor biosphere linked to global hydrothermal systems; TAIGA Concept. Tokyo: Springer, pp. 639–666. doi: 10.1007/978-4-431-54865-2_51.Google Scholar
Lindsay, D.J., Grossmann, M.M., Nishikawa, J., Bentlage, B. and Collins, A.G. (2015b) DNA barcoding of pelagic cnidarians: status and future prospects. Bulletin of the Plankton Society of Japan 62, 39–43.Google Scholar
Mapstone, G.M. (2009) Siphonophora (Cnidaria: Hydrozoa) of Canadian Pacific waters. Ottawa: NRC Research Press.Google Scholar
Mapstone, G.M. (2014) Global diversity and review of Siphonophorae (Cnidaria: Hydrozoa). PLoS ONE 9, e87737. doi: 10.1371/journal.pone.0087737.Google Scholar
Margulis, R.Y. (1980) On the vertical distribution of siphonophores in the world's oceans. In Naumov, D.V. and Stepanjants, S.D. (eds) The theoretical and practical importance of coelenterates. Leningrad: Zoological Institute, Russian Academy of Sciences, pp. 60–65.Google Scholar
Margulis, R.Y. (1982) Two new Siphonophores from Antarctic (Hydrozoa, Siphonophora). Zoologicheskii Zhurnal 61, 777–780.Google Scholar
Margulis, R.Y. (1992) Siphonophora from the Indian Sector of the Atlantic. Antarktika 30, 125–134.Google Scholar
Mills, C.E. (2001) Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451, 55–68.Google Scholar
Moser, F. (1925) Die Siphonophoren der Deutschen Südpolar-Expedition, 1901–1903. Deutsche Südpolar-Expedition 1901–1903 17 (Zoologie Band 9), 1–541.Google Scholar
OBIS (Ocean Biogeographic Information system): http://www.iobis.org/explore/#/taxon/695897 (Bargmannia elongata); accessed via IOBIS.org on 2.8.2017.Google Scholar
Ortman, B.D., Bucklin, A., Pagès, F. and Youngbluth, M. (2010) DNA barcoding the Medusozoa using mtCOI. Deep Sea Research Part II 57, 2148–2156.Google Scholar
Pagès, F. and Gili, J.M. (1989) Siphonophores (Cnidaria, Hydrozoa) collected during the “Magga Dan” Expedition (1966–67) from Africa to Antarctica. Scientia Marina 53, 53–57.Google Scholar
Pagès, F. and Kurbjeweit, F. (1994) Vertical−distribution and abundance of mesoplanktonic medusae and siphonophores from the Weddell Sea, Antarctica. Polar Biology 14, 243–251.Google Scholar
Pagès, F. and Orejas, C. (1999) Medusae, siphonophores and ctenophores of the Magellan region. Scientia Marina 63, 51–57.Google Scholar
Pagès, F. and Schnack-Schiel, S.B. (1996) Distribution patterns of the mesozooplankton, principally siphonophores and medusae, in the vicinity of the Antarctic Slope Front (eastern Weddell Sea). Journal of Marine Systems 9, 231–248.Google Scholar
Pagès, F., Pugh, P.R. and Gili, J.-M. (1994) Macro- and megaplanktonic cnidarians collected in the eastern part of the Weddell Gyre during summer 1979. Journal of the Marine Biological Association of the United Kingdom 74, 873–894.Google Scholar
Pakhomov, Y.A., Grachev, D.G. and Trotsenko, B.G. (1994) Distribution and composition of macroplankton communities in the Lazarev Sea (Antarctic). Oceanology of the Russian Academy of Sciences 33, 635–642.Google Scholar
Palma, S. (1986) Sifonoforos fisonectes colectados frente a la costa de Valparaiso. Investigaciones Marinas 14, 69–78.Google Scholar
Palma, S. (2006) Distribución y abundancia de zooplanc-ton en canales y fiordos australes. In Silva, N. and Palma, S. (eds) Avances en el conocimiento oceanógrafico de las aguas interiores chilenas, Puerto Montt a cabo de Hornos. Valparaíso: Comité Oceanógrafico Nacional-Pontificia Universidad Católica de Valparaíso, pp. 107–113.Google Scholar
Palma, S. and Aravena, G. (2001) Distribución de quetognatos, eufáusidos y sifonóforos en la región Magallánica. Revista Ciencia y Tecnología del Mar 24, 47–59.Google Scholar
Palma, S. and Rosales, S. (1997) Sifonóforos epipelágicos de los canales australes de Chile (41°30′−46°40′S). Ciencia y Tecnología del Mar 20, 125–146.Google Scholar
Palma, S., Retamal, M.C., Silva, N. and Canepa, A. (2016) Siphonophores in fjords and channels in southern Patagonia: biodiversity, spatial distribution and environmental association. Journal of the Marine Biological Association of the United Kingdom 98, 245–259. doi: 10.1017/S0025315416001302.Google Scholar
Panasiuk-Chodnicka, A. and Żmijewska, M.I. (2010) Cnidaria from Croker Passage (Antarctic Peninsula) with a special focus on Siphonophorae. Polar Biology 33, 1131–1143.Google Scholar
Panasiuk-Chodnicka, A., Żmijewska, M.I. and Mańko, M.K. (2014) Vertical migration of Siphonophora (Cnidaria) and their productivity in the Croker Passage, the Antarctic. Polish Polar Research 35, 115–131.Google Scholar
Pugh, P.R. (1984) The diel migrations and distributions within a mesopelagic community in the north east Atlantic. 7. Siphonophores. Progress in Oceanography 13, 46–489.Google Scholar
Pugh, P.R. (1999a) A review of the genus Bargmannia Totton, 1954 (Siphonophorae, Physonecta, Pyrostephidae). Bulletin of the Natural History Museum, Zoology Series 65, 51–72.Google Scholar
Pugh, P.R. (1999b) Siphonophorae. In Boltovskoy, D. (ed.) South Atlantic zooplankton. Leiden: Backhuys Publishers, pp. 467–511.Google Scholar
Pugh, P.R. and Gasca, R. (2009) Siphonophorae (Cnidaria) of the Gulf of Mexico. In Felder, D.L. and Camp, D.K. (eds) Gulf of Mexico: origins, waters, and biota. Vol. 1, Biodiversity. College Station, TX: Texas A&M Press, pp. 395–402.Google Scholar
Pugh, P.R., Pagès, F. and Boorman, B. (1997) Vertical distribution and abundance of pelagic cnidarians in the Eastern Weddell Sea, Antarctica. Journal of the Marine Biological Association of the United Kingdom 77, 341–360.Google Scholar
Ratnasingham, S. and Hebert, P.D. (2007) BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.Google Scholar
Shearer, T.L., Van Oppen, M.J.H., Romano, S.L. and Wörheide, G. (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11, 2475–2487.Google Scholar
Toda, R., Moteki, M., Ono, A., Horimoto, N., Tanaka, Y. and Ishimaru, T. (2010) Structure of the pelagic cnidarian community in Lützow–Holm Bay in the Indian sector of the Southern Ocean. Polar Science 4, 387–404.Google Scholar
Toda, R., Lindsay, D.J., Fuentes, V.L. and Moteki, M. (2014) Community structure of pelagic cnidarians off Adélie Land, East Antarctica, during austral summer 2008. Polar Biology 37, 269–289.Google Scholar
Totton, A.K. (1941) New species of the siphonophoran genus Lensia Totton, 1932. The Annals and Magazine of Natural History Ser. 11 8, 145–168.Google Scholar
Totton, A.K. (1954) Siphonophora of the Indian Ocean together with systematic and biological notes on related specimens from other oceans. Discovery Reports 27, 1–162.Google Scholar
Totton, A.K. and Bargmann, M.E. (1965) A synopsis of the Siphonophora. London: British Museum (Natural History).Google Scholar
Zheng, L., He, J., Lin, Y., Cao, W. and Zhang, W. (2014) 16S rRNA is a better choice than COI for DNA barcoding hydrozoans in the coastal waters of China. Acta Oceanologica Sinica 33, 55–76.Google Scholar
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