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Issue: Vol. 4433 No. 3: 13 Jun. 2018
Type: Article
Published: 2018-06-13
DOI: 10.11646/zootaxa.4433.3.10
Page range: 561–573
Abstract views: 66
PDF downloaded: 1

Two new European species of the marine genus Tubificoides (Annelida: Clitellata: Naididae) with notes on the morphology of T. pseudogaster (Dahl, 1960)

Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON M5S 2C6 , Canada Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 2B4, Canada
Department of Biological and Environmental Sciences, University of Gothenburg, Box 463, SE-405 35 Göteborg, Sweden
Annelida Tubificoides Tubificinae pseudo-cryptic speciation new species genetic variation integrative taxonomy

Abstract

Two new species of Tubificoides (subfamily Tubificinae), T. charlotteae n. sp. and T. mackiei n. sp., are described based on morphological analyses. Both species were flagged as potentially cryptic in a previous investigation, based on both mitochondrial and nuclear sequence data. Tubificoides charlotteae n. sp., known only from an intertidal site in southern Spain, is characterized by the lack of cuticular papillation, the possession of several needle-like hair chaetae in dorsal bundles, a cone-shaped penis sheath, and a rather large, muscular penial sac. It strongly resembles the north-west European, largely sublittoral species T. amplivasatus, but differs from this species in terms of body size, width of vas deferens, and the shape and size of both the ejaculatory duct and penial sac. Tubificoides mackiei n. sp., collected from the southeast coast of Norway and the west coast of Sweden, is characterized by the lack of cuticular papillae and hair chaetae, and the possession of a rather long penis sheath with a wide terminal opening. It shares several morphological features with the sympatric species Tubificoides pseudogaster, but is distinguished from the latter by the detailed morphology and length of the penis sheaths, the width of the atrium, and the lower maximal number of bifid chaetae in dorsal preclitellar bundles. The utility of an integrative comparative approach, combining molecules and morphology, for the identification and delineation of new taxa within Tubificoides is briefly discussed.

 

References

  1. Achurra, A., Creuze de Chatelliers, M. & Rodriguez, P. (2012) Troglodrilus jugeti n. sp. (Annelida, Clitellata, Tubificinae), a new stygobiont oligochaete species from south-western Europe. Zootaxa, 3229, 35–46.

    Achurra, A., Rodriguez, P. & Erséus, C. (2015) Pseudo-cryptic speciation in the subterranean medium: a new species of Stylodrilus Claparède, 1862, with a revision of the status of Bichaeta Bretscher, 1900 (Annelida, Clitellata, Lumbriculidae). Zoologischer Anzeiger, 257, 71–86.
    https://doi.org/10.1016/j.jcz.2015.05.003

    Baker, H.R. (1980) A redescription of Tubificoides pseudogaster (Dahl) (Oligochaeta: Tubificidae). Transactions of the American Microscopical Society, 99 (3), 337–342.
    https://doi.org/10.2307/3226011

    Baker, H.R. (1983) New species of Tubificoides Lastockin (Oligochaeta; Tubificidae) from the Pacific Northeast and the Arctic. Canadian Journal of Zoology, 61 (6), 1270–1283.
    https://doi.org/10.1139/z83-171

    Baker, H.R. (1984) Diversity and zoogeography of marine Tubificidae (Annelida, Oligochaeta) with notes on variation in widespread species. Hydrobiologia, 115 (1), 191–196.
    https://doi.org/10.1007/BF00027916

    Bamber, R.N. & Spencer, J.F. (1984) The benthos of a coastal power station thermal discharge canal. Journal of the Marine Biological Association of the UK, 64 (3), 603–623.
    https://doi.org/10.1017/S0025315400030290

    Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K., Meier, R., Winker, K., Ingra, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution, 22 (3), 148–155.
    https://doi.org/10.1016/j.tree.2006.11.004

    Brinkhurst, R.O. (1981) A contribution to the taxonomy of the Tubificinae (Oligochaeta: Tubificidae). Proceedings of the Biological Society of Washington, 94 (4), 1048–1067.

    Brinkhurst, R.O. (1985) A further contribution to the taxonomy of the genus Tubificoides Lastockin (Oligochaeta: Tubificidae). Canadian Journal of Zoology, 63 (2), 400–410.
    https://doi.org/10.1139/z85-061

    Brinkhurst, R.O. (1986) Taxonomy of the genus Tubificoides Lastockin (Oligochaeta, Tubificidae): species with bifid setae. Canadian Journal of Zoology, 64 (6), 1270–1279.
    https://doi.org/10.1139/z86-189

    Brinkhurst, R.O. & Baker, H.R. (1979) A review of the marine Tubificidae (Oligochaeta) of North America. Canadian Journal of Zoology, 57 (8), 1553–1569.
    https://doi.org/10.1139/z79-203

    Buckley, T.R., James, S., Allwood, J., Bartlam, S., Howitt, R. & Prada, D. (2011) Phylogenetic analysis of New Zealand earthworms (Oligochaeta: Megascolecidae) reveals ancient clades and cryptic taxonomic diversity. Molecular Phylogenetics and Evolution, 58 (1), 85–96.
    https://doi.org/10.1016/j.ympev.2010.09.024

    Chang, C.-H., Lin, S.-M. & Chen, J.-H. (2008) Molecular systematics and phylogeography of the gigantic earthworms of the Metaphire formosae species group (Clitellata, Megascolecidae). Molecular Phylogenetics and Evolution, 49 (3), 958–968.
    https://doi.org/10.1016/j.ympev.2008.08.025

    Claparède, E.R. (1862) Recherches anatomiques sur les oligochetes. Memoirs of the Society of Physics and Natural History Geneva, 16, 217–291.

    Cook, D.G. (1969) Peloscolex dukei n.sp. and P. aculeatus n.sp. (Oligochaeta, Tubificidae) from the North-west Atlantic, the latter being from abyssal depths. Transactions of the American Microscopical Society, 88 (4), 492–497.
    https://doi.org/10.2307/3224243

    Cook, D.G. (1970) Bathyal and abyssal Tubificidae (Annelida, Oligochaeta) from the Gay Head–Bermuda transect, with descriptions of new genera and species. Deep–Sea Research, 17 (6), 973–981.
    https://doi.org/10.1016/0011-7471(70)90048-3

    Dahl, I.O. (1960) The oligochaete fauna of 3 Danish brackish water areas (taxonomic and biological observations). Meddelelser fra Danmarks Fiskeri- og Havundersøgelser, New Series, 26, 1–20.

    De Wit, P. & Erséus, C. (2010) Genetic variation and phylogeny of Scandinavian species of Grania (Annelida: Clitellata: Enchytraeidae), with the discovery of a cryptic species. Journal of Zoological Systematics and Evolutionary Research, 48 (4), 285–293.
    https://doi.org/10.1111/j.1439-0469.2010.00571.x

    De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56 (6), 879–886.
    https://doi.org/10.1080/10635150701701083

    Donnelly, R.K., Harper, G.L., Morgan, A.J., Orozco-Terwengel, P., Pinto-Juma, G.A. & Bruford, M.W. (2013) Nuclear DNA recapitulates the cryptic mitochondrial lineages of Lumbricus rubellus and suggests the existence of cryptic species in an ecotoxicological soil sentinel. Biological Journal of the Linnean Society, 110 (4), 780–795.
    https://doi.org/10.1111/bij.12171

    d’Udekem, J. (1855) Histoire naturelle du Tubifex des ruisseaux. Mémoires Couronnés des Savantes Etrangers de l’Académie Royal de Belgique, 26, 1–38.

    Erséus, C. (1975) Peloscolex amplivasatus sp.n. and Macroseta rarisetis gen. et sp.n. (Oligochaeta, Tubificidae) from the West coast of Norway. Sarsia, 58 (1), 1–8.
    https://doi.org/10.1080/00364827.1975.10411274

    Erséus, C. (1976) Marine subtidal Tubificidae and Enchytraeidae (Oligochaeta) of the Bergen area, Western Norway. Sarsia, 62 (1), 25–48.
    https://doi.org/10.1080/00364827.1976.10411312

    Erséus, C. & Gustafsson, D. (2009) Cryptic speciation in clitellate model organisms. In: Shain, D. (Ed.), Annelids in Modern Biology. John Wiley & Sons, Hoboken, New Jersey, pp. 31–46.
    https://doi.org/10.1002/9780470455203.ch3

    Erséus, C. & Kvist, S. (2007) COI variation in Scandinavian marine species of Tubificoides (Annelida: Clitellata: Tubificidae). Journal of the Marine Biological Association of the UK, 87 (5), 1121–1126.
    https://doi.org/10.1017/S0025315407055610

    Erséus, C., Wetzel, M.J. & Gustavsson, L. (2008) ICZN rules—a farewell to Tubificidae (Annelida, Clitellata). Zootaxa, 1744 (1), 66–68.
    https://doi.org/10.11646/zootaxa.1744.1.7

    Gustafsson, D.R., Price, D.A. & Erséus, C. (2009) Genetic variation in the popular lab worm Lumbriculus variegatus (Annelida: Clitellata: Lumbriculidae) reveals cryptic speciation. Molecular Phylogenetics and Evolution, 51 (2), 182–189.
    https://doi.org/10.1016/j.ympev.2008.12.016

    Hebert, P.D.N., Penton E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences USA, 101 (41), 14812–14817.
    https://doi.org/10.1073/pnas.0406166101

    Hebert, P.D.N., Ratnasingham, S. & deWaard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B (Biological Sciences), 270 (1512), 96–99. [S96–S99]
    https://doi.org/10.1098/rsbl.2003.0025

    Helgason, G.V. & Erséus, C. (1987) Three new species of Tubificoides (Oligochaeta, Tubificidae) from the North–west Atlantic and notes on geographic variation in the circumpolar T. kozloffi. Sarsia, 72 (2), 159–169.
    https://doi.org/10.1080/00364827.1987.10419713

    Holmquist, C. (1978) Revision of the genus Peloscolex (Oligochaeta, Tubificidae). 1. Morphological and anatomical scrutiny; with discussion on the generic level. Zoologica Scripta, 7, 187–209.
    https://doi.org/10.1111/j.1463-6409.1978.tb00602.x

    Holmquist, C. (1979) Revision of the genus Peloscolex (Oligochaeta, Tubificidae). 2. Scrutiny of the species. Zoologica Scripta, 8, 37–60.
    https://doi.org/10.1111/j.1463-6409.1979.tb00618.x

    Hrabě, S. (1966) New or insufficiently known species of the family Tubificidae. Publicationes Facultatis Scientarium Universitatis J. E. Purkyně, Brno, 470, 57–76.

    James, S. W., Porco, D., Decaens, T., Richard, B., Rougerie, R. & Erséus, C. (2010) DNA barcoding reveals cryptic diversity in Lumbricus terrestris L., 1758 (Clitellata): resurrection of L. herculeus (Savigny, 1826). PLoS ONE, 5, e15629.
    https://doi.org/10.1371/journal.pone.0015629

    Juget, J., des Chatelliers, M. & Rodriguez, P. (2006) Troglodrilus (Annelida, Oligochaeta, Tubificidae), a new genus from subterranean habitats in southwestern Europe. Hydrobiologia, 564, 7–17.
    https://doi.org/10.1007/s10750-005-1703-2

    Kawauchi, G.Y. & Giribet, G. (2014) Sipunculus nudus Linnaeus, 1766 (Sipuncula): cosmopolitan or a group of pseudo-cryptic species? An integrated molecular and morphological approach. Marine Ecology, 35 (4), 478–491.
    https://doi.org/10.1111/maec.12104

    Kvist, S., Dreyer, J. & Erséus, C. (2008) Two new species of Tubificoides (Annelida: Clitellata: Naididae) from the Blake Ridge methane seep in the North–west Atlantic Ocean. Proceedings of the Biological Society of Washington B, 121 (4), 531–540.
    https://doi.org/10.2988/08-14.1

    Kvist, S., Sarkar, I.N. & Erséus, C. (2010) Genetic variation and phylogeny of the cosmopolitan marine genus Tubificoides (Annelida: Clitellata: Naididae: Tubificinae). Molecular Phylogenetics and Evolution, 57 (2), 687–702.
    https://doi.org/10.1016/j.ympev.2010.08.018

    Laakso, M. (1969) Oligochaeta from brackish water near Tvärminne, south-west Finland. Annales Zoologici Fennici, 6 (1), 98–111.

    Lamarck, J.B. (1816) Histoire naturelle des animaux sans vertèbres 3. Verdière, Paris, 585 pp.

    Lastockin, D.A. (1937) New species of Oligochaeta limicola in the European part of the U.S.S.R. Compte Rendus (Doklady) de l’Académie des Sceinces de l’URSS, 17, 233–235.

    Leidy, J. (1851) Description of new genera of Vermes. Proceedings of the Academy of Natural Sciences of Philadelphia, 5, 239–244.

    Liu, Y., Fend, S.V., Martinsson, S. & Erséus, C. (2017) Extensive cryptic diversity in the cosmopolitan sludge worm Limnodrilus hoffmeisteri (Clitellata, Naididae). Organisms Diversity & Evolution, 17 (2), 477–495.
    https://doi.org/10.1007/s13127-016-0317-z

    Martinsson, S., Achurra, A., Svensson, M. & Erséus, C. (2013) Integrative taxonomy of the freshwater worm Rhyacodrilus falciformis s.l. (Clitellata: Naididae), with the description of a new species. Zoologica Scripta, 42 (6), 612–622.

    Martinsson, S. & Erséus, C. (2014) Cryptic diversity in the well–studied terrestrial worm Cognettia sphagnetorum (Clitellata: Enchytraeidae). Pedobiologia, 57 (1), 27–35.
    https://doi.org/10.1016/j.pedobi.2013.09.006

    Martinsson, S. & Erséus, C. (2017) Cryptic speciation and limited hybridization within Lumbricus earthworms (Clitellata: Lumbricidae). Molecular Phylogenetics and Evolution, 106 (2017), 18–27.
    https://doi.org/10.1016/j.ympev.2016.09.011

    Matamoros, L., Rota, E. & Erséus, C. (2012) Cryptic diversity among the achaetous Marionina (Annelida, Clitellata, Enchytraeidae). Systematics and Biodiversity, 10 (4), 509–525.
    https://doi.org/10.1080/14772000.2012.723640

    Michaelsen, W. (1926) Oligochaeten aus dem Ryck bei Greifswald und von benachbarten Meeresgebieten. Mitteilungen aus den Hamburgischen Zoologischen Museum und Institut, 42, 21–29.

    Milligan, M.R. (1996) Identification manual for the aquatic Oligochaeta of Florida. Volume II. Estuarine and nearshore marine oligochaetes. Final Report for DEP Contract Number WM550. Florida Department of Environmental Protection, Division of Water Facilities, Tallahassee, Florida, 239 pp.

    Moura, C.J., Harris, D.J., Cunha, M.R. & Rogers, A.D. (2008) DNA barcoding reveals cryptic diversity in marine hydroids (Cnidaria, Hydrozoa) from coastal environments. Zoologica Scripta, 37 (1), 93–108.

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

    Ratnasingham, S. & Hebert, P.D.N. (2007) BOLD: the barcode of life data system. Molecular Ecology Resources, 7 (3), 355–364.
    https://doi.org/10.1111/j.1471-8286.2007.01678.x

    Reise, K., Herre, E, & Sturm, M. (1994) Biomass and abundance of macrofauna in intertidal sediments of Königshafen in the northern Wadden Sea. Helgoländer Meeresuntersuchungen, 48, 201–215.
    https://doi.org/10.1007/BF02367036

    Sarkar, I.N., Planet, P.J., Bael, T.E., Stanley, S.E., Siddall, M., DeSalle, R. & Figurski, D.H. (2002) Characteristic attributes in cancer microarrays. Journal of Biomedical Informatics, 35 (2), 111–122.
    https://doi.org/10.1016/S1532-0464(02)00504-X

    Savigny, J.C. (1822) Système des annélides, principalement de celles des côtes de l’Égypte et de la Syrie, offrant les caractères tant distinctifs que naturels des ordres, familles et genres, avec la description des espèces. Description de l’Egypte. Histoire Naturelle, Paris, 1, 1–128.

    Smith, M.A., Fisher, B.L. & Hebert, P.D.N. (2005) DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar. Philosophical Transactions of the Royal Society B: Biological Sciences, 360 (1462), 1825–1834.
    https://doi.org/10.1098/rstb.2005.1714

    Takashima, Y. & Mawatari, S.F. (1996) Marine Tubificidae (Oligochaeta) from Hokkaido, northern Japan, with descriptions of two new species. Species Diversity, 1, 55–70.
    https://doi.org/10.12782/specdiv.1.55

    Witt, J.D.S., Threloff, D.L. & Hebert, P.D.N. (2006) DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Molecular Ecology, 15 (10), 3073–3082.
    https://doi.org/10.1111/j.1365-294X.2006.02999.x