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Type: Article
Published: 2018-08-01
Page range: 1–34
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Six new species of Macellicephala (Annelida: Polynoidae) from the Southern Ocean and south Atlantic with re-description of type species

Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK.
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK. School of Environmental Science, University of Liverpool, L69 3BX, Liverpool, UK.
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK.
Species descriptions Morphology Monophyly Molecular phylogeny 16S 18S COI Annelida

Abstract

Increased sampling efforts in unexplored regions of the Southern Ocean (including depths >500 m) combined with the use of an epibenthic sledge resulted in a large collection of mobile, scale-bearing worms from the family Polynoidae Kinberg, 1856. The greatest taxonomic novelty was found in the genus Macellicephala McIntosh, 1885, the type genus of the exclusively deep-sea polynoid sub-family Macellicephalinae Hartmann-Schröder, 1971. Recently collected material from the Amundsen Sea led to discovery of four new species based on morphology and COI, 16S and 18S genes—Macellicephala gloveri sp. nov., M. linseae sp. nov., M. patersoni sp. nov. and M. brenesorum sp. nov. The holotype of type taxon Macellicephala mirabilis McIntosh, 1885 as well as historic material of Macellicephala collected from the Southern Ocean enabled comparison with the modern material. As a result, Macellicephala mirabilis is re-defined, and two new species, M. monroi sp. nov. and M. macintoshi sp. nov., are erected from the historic material previously ascribed to M. mirabilis. Additionally, DNA-suitable specimens assigned to M. monroi sp. nov. were collected from the Scotia Sea. Genetic data enabled the first test of the monophyly of Macellicephala. Based on current taxa coverage, these taxa form a well-supported monophyletic group as recovered by Bayesian and Maximum Likelihood analyses of our combined genetic dataset. In addition, the analysis shows strong support of a clade comprising Macellicephala and other exclusively deep-sea groups (including cave-dwelling taxa).

References

  1. Barnich, R. (2011) Identification of scale worms in British and Irish waters. Senckenberg-Forschungsinstitut und Naturmuseum, Frankfurt, 52 pp.

    Brandt, A., De Broyer, C., Gooday, A.J., Hilbig, B. & Thomson, M.R. (2004) Introduction to ANDEEP (ANtarctic benthic DEEP-sea biodiversity: colonization history and recent community patterns) - a tribute to Howard L. Sanders. Deep Sea Research Part II: Topical Studies in Oceanography, 51 (14), 1457–1465.
    https://doi.org/10.1016/j.dsr2.2004.08.006

    Brandt, A., Gooday, A.J., Brandão, S.N., Brix, S., Brökeland, W., Cedhagen, T., Choudhury, M., Cornelius, N., Danis, B., De Mesel, I. & Diaz, R.J. (2007) First insights into the biodiversity and biogeography of the Southern Ocean deep-sea. Nature, 447 (7142), 307.
    https://doi.org/10.1038/nature05827

    Brasier, M.J., Wiklund, H., Neal, L., Jeffreys, R., Linse, K., Ruhl, H. & Glover, A.G. (2016) DNA barcoding uncovers cryptic diversity in 50% of deep-sea Antarctic polychaetes. Royal Society Open Science, 3 (11), 160432.
    https://doi.org/10.1098/rsos.160432

    Brenke, N. (2005) An epibenthic sledge for operations on marine soft bottom and bedrock. Marine Technology Society Journal, 39 (2), 10–21.
    https://doi.org/10.4031/002533205787444015

    Carr, C.M., Hardy, S.M., Brown, T.M., Macdonald, T.A. & Hebert, P.D. (2011) A trioceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS One, 6 (7), e22232.
    https://doi.org/10.1371/journal.pone.0022232

    Chamberlin, R.V. (1919) The Annelida Polychaeta [Albatross Expeditions]. Memoirs of the Museum of Comparative Zoology at Harvard College, 48, 1–514.

    Chernomor, O., von Haeseler, A. & Minh, B.Q. (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology, 65, 997–1008. https://doi.org/10.1093/sysbio/syw037

    Cohen, B.L., Gawthrop, A. & Cavalier-Smith, T. (1998) Molecular phylogeny of brachiopods and phoronids based on nuclear-encoded small subunit ribosomal RNA gene sequences. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 353 (1378), 2039–2061.
    https://doi.org/10.1098/rstb.1998.0351

    Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797.
    https://doi.org/10.1093/nar/gkh340

    Folmer, O., Hoeh, W.R., Black, M.B. & Vrijenhoek, R.C. (1994) Conserved primers for PCR amplification of mitochondrial DNA from different invertebrate phyla. Molecular Marine Biology and Biotechnology, 3, 294–299.

    Glover, A.G., Goetze, E., Dahlgren, T.G. & Smith, C.R. (2005) Morphology, reproductive biology and genetic structure of the whale‐fall and hydrothermal vent specialist, Bathykurila guaymasensis (Annelida: Polynoidae). Marine Ecology, 26 (3–4), 223–234.
    https://doi.org/10.1111/j.1439-0485.2005.00060.x

    Glover, A.G., Dahlgren, T.G., Wiklund, H., Mohrbeck, I. & Smith, C.R. (2015) An endto-end DNA taxonomy methodology for benthic biodiversity survey in the Clarion-Clipperton Zone, central Pacific abyss. Journal of Marine Science and Engineering, 4 (1), 2. https://doi.org/10.3390/jmse4010002

    Gonzalez, B.C., Martinez, A., Borda, E., Iliffe, T.M., Eibye Jacobsen, D. & Worsaae, K. (2017a) Phylogeny and systematics of Aphroditiformia. Cladistics, 34 (3), 1–35.
    https://doi.org/10.1111/cla.12202

    Gonzalez, B.C., Martinez, A., Borda, E., Iliffe, T.M., Fontaneto, D. & Worsaae, K. (2017b) Genetic spatial structure of an anchialine cave annelid indicates connectivity within-but not between-islands of the Great Bahama Bank. Molecular Phylogenetics and Evolution, 109, 259–270.
    https://doi.org/10.1016/j.ympev.2017.01.003

    Griffiths, H.J. (2010) Antarctic marine biodiversity-what do we know about the distribution of life in the Southern Ocean? PloS One, 5 (8), e11683.
    https://doi.org/10.1371/journal.pone.0011683

    Hartman, O. (1967) Polychaetous annelids collected by the USNS Eltanin and Staten Island cruises, chiefly from Antarctic Seas. Allan Hancock Monographs in Marine Biology, 2, 1–387.

    Hartmann-Schröder, G. (1971) Annelida, Borstenwurmer, Polychaeta. Die Tierwelt Deutschlands und der Angrenzenden Meeresteile, 58, 1–594.

    Hartmann-Schröder, G. (1974) Die Unterfamilie Macellicephalinae. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 71, 75–85.

    Hillger, K.A. & Reish, D.J. (1970) The Effect of Temperature on the Setal Characteristics in Polynoidae (Annelidae: Polychaeta). Bulletin of the Southern California Academy of Sciences, 69 (2), 87–99.

    Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution, 35 (2), 518–522.
    https://doi.org/10.1093/molbev/msx281

    Hutchings, P.A. (2000) Family Polynoidae. In: Beesley, P.L., Ross, G.J. & Glasby, C.J. (Eds.), Polychaetes & Allies: The Southern Synthesis. Vol. 4. CSIRO publishing, Melbourne, pp. 152–157.

    Kaiser, S., Barnes, D.K., Sands, C.J. & Brandt, A. (2009) Biodiversity of an unknown Antarctic Sea: assessing isopod richness and abundance in the first benthic survey of the Amundsen continental shelf. Marine Biodiversity, 39 (1), 27.
    https://doi.org/10.1007/s12526-009-0004-9

    Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589.
    https://doi.org/10.1038/nmeth.4285

    Katoh, K., Misawa, K., Kuma, K.I. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic acids research, 30 (14), 3059–3066.
    https://doi.org/10.1093/nar/gkf436

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649.
    https://doi.org/10.1093/bioinformatics/bts199

    Kinberg, J.G.H. (1856) Nya slägten och arter af Annelider. Öfversigt af Königlich Vetenskaps-Akademiens Förhhandlingar Stockholm, 12 (9–10), 381–388.

    Levenstein, R.Y. (1975) The Polychaetous Annelids of the Deep-Sea Trenches of the Atlantic Sector of the Antarctic Ocean. Transactions of the P.P.Shirov Institute of Oceanology Academy of Sciences of the USSR, 103, 119–142.

    Levenstein, R.Y. (1978) Polychaetes of the Family Polynoidae (Polychaeta) from the Deep-Water Trenches of the Western Part of the Pacific. Transactions of the P.P.Shirov Institute of Oceanology Academy of Sciences of the USSR, 112, 162–173.

    Levinsen, G.M.R. (1887) Kara-Havets Ledorme (Annulata). In: Lutken, C.F. (Ed.), Djimphna-Togtets Zoologiske-botaniske Udbytte. J. Hagerup, Kobenhaven, pp. 288–303.

    Linse, K. (2008) The BIOPEARL expedition to the Scotia Sea in 2006. Antarctic Science, 20 (3), 211.
    https://doi.org/10.1017/S095410200800120X

    Linse, K., Griffiths, H.J., Barnes, D.K., Brandt, A., Davey, N., David, B., De Grave, S., Eléaume, M., Glover, A.G., Hemery, & Mah, C. (2013) The macro-and megabenthic fauna on the continental shelf of the eastern Amundsen Sea, Antarctica. Continental Shelf Research, 68, 80–90.
    https://doi.org/10.1016/j.csr.2013.08.012

    Loshamn, A.A. (1981) Descriptions of five polynoid species (Polychaeta) from the coasts of Norway and Sweden, including three new species, one new genus and one new generic name. Zoologica Scripta, 10 (1), 5–13.
    https://doi.org/10.1111/j.1463–6409.1981.tb00480.x

    Maddison, W.P & Maddison, D.R (2018) Mesquite: a modular system for evolutionary analysis. Version 3.40. Available from: http://mesquiteproject.org (accessed 15 January 2018)

    Malmgren, A.J. (1865) Nordiska Hafs-Annulater. Öfversigt af Königlich Vetenskapsakademiens Förhandlingar, Stockholm, 22 (1), 51–110.

    McIntosh, W.C. (1885) Report on the Annelida Polychaeta collected by HMS Challenger during the years 1873-76. Report of the Scientific Results of the Voyage of HMS Challenger 1873–76, 12, 1–554.

    McIntosh, W.C. (1897) Notes from the Gatty Marine Laboratory, St. Andrews. No. 18. 1. On the phosphorescence of Gattyana (Nychia) cirrosa. Pallas Annals and Magazine of Natural History, 20 (6), 167–178.

    Mclntosh, W.C. (1905) Marine Annelids (Polychaeta) of South Africa, Part 2. Marine Investigations in South Africa, 3, 57–92.

    Medlin, L., Elwood, H.J., Stickel, S. & Sogin, M.L. (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene, 71 (2), 491–499.
    https://doi.org/10.1016/0378-1119(88)90066-2

    Monro, C.C.A. (1930) Polychaete worms. Discovery Reports, 2, 1–222.

    Monro, C.C.A. (1936) Polychaete Worms, II. Discovery Reports, 12, 59–198.

    Moore, J.P. (1910) The polychaetous annelids dredged by the U.S.S. ''Albatross'' off the coast of Southern California in 1904: II. Polynoidae, Aphroditidae and Segaleonidae. Proceedings of the Academy of Natural Sciences of Philadelphia, 62, 328–402, pls.XXVIII–XXXIII.

    Moreau, C., Linse, K., Griffiths, H., Barnes, D., Kaiser, S., Glover, A., Sands, C., Strugnell, J., Enderlein, P. & Geissler, P. (2013) Amundsen Sea Mollusca from the BIOPEARL II expedition. ZooKeys, 294, 1–8.
    https://doi.org/10.3897/zookeys.294.4796

    Neal, L., Barnich, R., Wiklund, H. & Glover, A.G. (2012) A new genus and species of Polynoidae (Annelida, Polychaeta) from Pine Island Bay, Amundsen Sea, Southern Ocean-a region of high taxonomic novelty. Zootaxa, 3542, 80–88.

    Neal, L., Wiklund, H., Muir, A.I., Linse, K. & Glover, A.G. (2014) The identity of juvenile Polynoidae (Annelida) in the Southern Ocean revealed by DNA taxonomy, with notes on the status of Herdmanella gracilis Ehlers sensu Augener. Memoirs of Museum Victoria, 71, 203–216.
    https://doi.org/10.24199/j.mmv.2014.71.16

    Neal, L., Linse, K., Brasier, M.J., Sherlock, E. & Glover, A.G. (2017) Comparative marine biodiversity and depth zonation in the Southern Ocean: evidence from a new large polychaete dataset from Scotia and Amundsen seas. Marine Biodiversity, 1–21.

    https://doi.org/10.1007/s12526-017-0735-y

    Nguyen, L.T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 321, 268–274.
    https://doi.org/10.1093/molbev/msu300

    Norlinder, E., Nygren, A., Wiklund, H. & Pleijel, F. (2012) Phylogeny of scale-worms (Aphroditiformia, Annelida), assessed from 18SrRNA, 28SrRNA, 16SrRNA, mitochondrial cytochrome c oxidase subunit I (COI), and morphology. Molecular Phylogenetics and Evolution, 65 (2), 490–500.
    https://doi.org/10.1016/j.ympev.2012.07.002

    Nygren, A. & Sundberg, P. (2003) Phylogeny and evolution of reproductive modes in Autolytinae (Syllidae, Annelida) Molecular Phylogenetics and Evolution, 29 (2), 235–249.

    https://doi.org/10.1016/S1055-7903(03)00095-2

    Nygren, A. (2014) Cryptic polychaete diversity: a review. Zoologica Scripta, 43 (2), 172–183.
    https://doi.org/10.1111/zsc.12044

    Pabis, K., Błażewicz-Paszkowycz, M., Joźwiak, P. & Barnes, D.K. (2015) Tanaidacea of the Amundsen and Scotia seas: an unexplored diversity. Antarctic Science, 27 (1), 19–30.
    https://doi.org/10.1017/S0954102014000303

    Palumbi, S.R. (1996) Nucleic acid II: The polymerase chain reaction. In: Hillis, D.M., Moritz, G. & Mable, B. (Eds.), Molecular systematics. Sinauer Associates, Sunderland, pp. 205–247.

    Pettibone, M.H. (1976) Revision of the Genus Macellicephala McIntosh and the Subfamily Macellicephalinae Hartmann-Schröder (Polychaeta, Polynoidae). Smithsonian Contributions to Zoology, 229, 1–71.

    Pettibone, M.H. (1985) Polychaete worms from a cave in the Bahamas and from experimental wood panels in deep water of the North Atlantic (Polynoidae: Macellicephalinae, Harmothoinae). Proceedings of the Biological Society of Washington, 98 (1), 127–149.

    Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular biology and evolution, 25 (7), 1253–1256.
    https://doi.org/10.1093/molbev/msn083

    Rambaut, A. & Drummond, A.J. (2007) Tracer. Version 1. 4. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 10 July 2017)

    Read, G. & Fauchald, K. (Ed.) (2018a) World Polychaeta database. Polynoidae Kinberg, 1856. Accessed through: World Register of Marine Species. Available from: http://www.marinespecies.org/aphia.php?p=taxdetails&id=939 (accessed 5 April 2018)

    Read, G. & Fauchald, K. (Ed.) (2018b) World Polychaeta database. Harmothoe Kinberg, 1856. Accessed through: World Register of Marine Species. Available from: http://www.marinespecies.org/aphia.php?p=taxdetails&id=129491 (accessed 5 April 2018)

    Reyss, D. (1971) Resultats scientifiques de la Campagne Polymede. II.—Polychetes Aphroditidae de profondeur en Mediterranee. Remarques systematiques et biogeographiques. Vie et Milieu, Série A, 22 (2), 243–258.

    Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
    https://doi.org/10.1093/sysbio/sys029

    Rouse, G.W. & Fauchald, K. (1997) Cladistics and polychaetes. Zoologica Scripta, 26 (2), 139–204.
    https://doi.org/10.1111/j.1463-6409.1997.tb00412.x

    Rouse, G. & Pleijel, F. (2001) Polychaetes. Oxford University Press, Oxford, 354 pp.

    Shields, M.A., Glover, A.G. & Wiklund, H. (2013) Polynoid polychaetes of the Mid-Atlantic Ridge and a new holothurian association. Marine Biology Research, 9 (5–6), 547–553.
    https://doi.org/10.1080/17451000.2012.749992

    Schüller, M. & Ebbe, B. (2014) Chapter 5 Polychaetes. In: De Broyer, C., Koubbi, P., Griffiths, H.J., Raymond, B., d'Udekem d'Acoz, C. & Van de Putte, A.P. (Ed.), Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Camebridge, pp. 134–137.

    Schüller, M., Ebbe, B. & Wagele, J.W. (2009) Community structure and diversity of polychaetes (Annelida) in the deep Weddell Sea (Southern Ocean) and adjacent basins. Marine Biodiversity, 39 (2), 95–108.
    https://doi.org/10.1007/s12526-009-0009-4

    Sjölin, E., Erseus, C. & Kallersjo, M. (2005) Phylogeny of Tubificidae (Annelida, Clitellata) based on mitochondrial and nuclear sequence data. Molecular Phylogenetics and Evolution, 35, 431–441.
    https://doi.org/10.1016/j.ympev.2004.12.018

    Støp-Bowitz, C. (1948) Polychaeta from the "Michael Sars" North Atlantic deep-sea expedition 1910. Report on the Scientific Results of the Michael Sars North Atlantic Deep-Sea Expedition, 5 (8), 1–91.

    Struck, T.H., Purschke, G. & Halanych, K.M. (2005) A scaleless scale worm: Molecular evidence for the phylogenetic placement of Pisione remota (Pisionidae, Annelida). Marine Biology Research, 1 (4), 243–253.
    https://doi.org/10.1080/17451000500261951

    Uschakov, P.V. (1957) On the polychaete worms fauna (Polychaeta) of the Arctic and Antarctic]. K faune mnogoshchetinkovikh chervei (Polychaeta) Arkitki i Antarktiki. Zoologicheskii zhurnal, 36 (11), 1659–1672.

    Uschakov, P.V. (1971) On a New Abyssal Species of Macellicephala Mclntosh (Polychaeta, Errantia) from the Aleutian Trench. In Fauna of the Kurile-Kamchatka Trench. Trudy Institut Okeanologii P.P. Shirshov Academiia Nauk SSSR, 92, 36–40.

    Wiklund, H., Nygren, A., Pleijel, F. & Sundberg, P. (2005) Phylogeny of Aphroditiformia (Polychaeta) based on molecular and morphological data. Molecular Phylogenetics and Evolution, 37 (2), 494–502.
    https://doi.org/10.1016/j.ympev.2005.07.005

    Wirén, A. (1907) Macellicephala violacea Levinsen, nebst Bemerkungen ueber deren Anatomie. Zoologiska Studier Tillägnade Prof. T. Tullberg, Uppsala, 20 pp. [pp. 289–308]

    Wu, B.L. & Wang, H.Y. (1987) Two new species of Polychaeta from South Ocean. Acta Zootaxonomica Sinica, 12 (1), 23–29.

    Zrzavý, J., Řiha, P., Pialek, L. & Janouškovec, J. (2009) Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evolutionary Biology, 9 (1), 189.
    https://doi.org/10.1186/1471-2148-9-189