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Type: Article
Published: 2018-02-21
Page range: 367–380
Abstract views: 79
PDF downloaded: 1

A new species of Enchytraeus (Enchytraeidae, Oligochaeta) from the profundal of Lake Van, the world's largest soda Lake (Turkey, East Anatolia)

Eskişehir Osmangazi University, Science and Art Faculty, Biology Department, Eskişehir-Turkiye.
Estonian University of Life Sciences, Centre for Limnology, Rannu 61117, Tartumaa, Estonia.
AllGenetics & Biology SL. Edificio CICA. Campus de Elviña s/n. E-15008 A Coruña, Spain.
AllGenetics & Biology SL. Edificio CICA. Campus de Elviña s/n. E-15008 A Coruña, Spain.
IfAB, Institute for Applied Soil Biology, Tomberg 24a, 22337 Hamburg, Germany. Universidad de A Coruña, Fac. Ciencias, GIBE, Evolutionary Biology Research Group. Edificio CICA. Campus de Elviña. E-15008 A Coruña, Spain.
Annelida Clitellata extremophile aquatic oligochaetes benthos integrated taxonomy Middle East

Abstract

Enchytraeus polatdemiri sp. nov. (Enchytaeidae, Oligochaeta) was discovered in the framework of a sampling campaign of the benthic invertebrate fauna of the hyperalkaline Lake Van in Eastern Anatolia, Turkey, the third-largest closed lake and the largest soda lake on Earth. It was the only oligochaete species found in all samples. DNA sequencing included a fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene, and a fragment of the nuclear histone 3 (H3) gene. For comparison, specimens from laboratory cultures of E. albidus Henle, 1837, a widespread and morphologically similar species, were sequenced as well. The new species differs from E. albidus in comparatively small body size, 2 or 3 chaetae per bundle, saddle-shaped clitellum, absence of a copulatory field between the male pores and vasa deferentia usually not extending beyond the clitellum. The individual gene trees of COI and H3, as well as the combined phylogenetic analysis of both trees, recovered Enchytraeus polatdemiri sp. nov. as a monophyletic group within the genus Enchytraeus, closely related to E. albidus, but with an average p-distance for COI of 14.5 %. E. polatdemiri sp. nov. may have evolved from a local population of Enchytraeus albidus, a species well-adapted to changing salinity conditions, or from a common ancestor into an extremophile species that dwells and reproduces in the profundal of a strongly alkaline soda lake.

 

References

  1. Arslan, N. (2006) Records of Aphanoneura and aquatic oligochaetes from Turkey. Fresenius Environmental Bulletin, 15 (4), 249–254.

    Arslan, N., Timm, T. & Erséus, C. (2007) The aquatic Oligochaeta (Annelida) of Balıkdamı wetland in Turkey, with descriptions of two new species of Phallodrilinae. Biologia, Bratislava, 62 (3), 323–334.
    https://doi.org/10.2478/s11756-007-0055-y

    ASTM (American Society for Testing and Materials) (2000) Standard guide for conducting laboratory soil toxicity or bioaccumulation tests with the lumbricid earthworm Eisenia fetida and the enchytraeid potworm Enchytraeus albidus. ASTM Guideline, No. E. 1676–1697.

    Ayten, Y. & Özgökçe, M.S. (2009) Van ve çevresinde bulunan Odonata türleri, yayılışları ve habitatları. YYÜ Tar Bil Derg, 19 (1), 1–9.

    Bruns, E., Egeler, P., Römbke, J., Scheffczyk, A. & Spoerlein, P. (2001) Bioaccumulation of lindane and hexachlorobenzene by the oligochaetes Enchytraeus luxuriosus and Enchytraeus albidus (Enchytraeidae, Oligochaeta, Annelida). Hydrobiologia, 463, 185–196.
    https://doi.org/10.1023/A:1013159810067

    Christensen, B. & Glenner, H. (2010) Molecular phylogeny of Enchytraeidae (Oligochaeta) indicates separate invasions of the terrestrial environment. Journal of Zoological Systematics and Evolutionary Research, 48 (3), 208–212.
    https://doi.org/10.1111/j.1439-0469.2009.00558.x

    Colgan, D.J., McLauchlan, A., Wilson, G.D.F., Livingston, S.P., Edgecombe, G.D., Macaranas, J., Cassis, G. & Gray, M.R. (1998) Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology, 46, 419–437.
    https://doi.org/10.1071/ZO98048

    Danulat, E. & Kempe, S. (1992) Nitrogenous waste excretion and accumulation of urea and ammonia in Chalcalburnus tarichi (Cyprinidae), endemic to the extremely alkaline Lake Van (Eastern Turkey). Fish Physiology and Biochemistry, 9, 377–386.
    https://doi.org/10.1007/BF02274218

    Degens, E.T. & Kurtman, F. (Eds.) (1978), The Geology of Lake Van. No. 169. Maden Tetkik Ve Arama Enstitüsü Yayınları, Ankara, 158 pp.

    deWaard, J.R., Ivanova, N.V., Hajibabaei, M., Hebert, P.D.N. (2008) Assembling DNA barcodes. In: Martin, C.C. (Ed.), Environmental Genomics. Methods in Molecular Biology, 410, pp. 275–294.
    https://doi.org/10.1007/978-1-59745-548-0_15

    Dursun, A. (2012) Additional records of Gerromorpha (Hemiptera: Heteroptera) and redescription of Rhagovelia nigricans nigricans (Burmeister,1835) from Anatolia (Turkey). Turkish Journal of Zoology, 36 (5), 652–661.

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

    Erséus, C., Rota, E., Matamoros, L. & De Wit, P. (2010) Molecular phylogeny of Enchytraeidae (Annelida, Clitellata). Molecular Phylogenetics and Evolution, 57, 849–858.
    https://doi.org/10.1016/j.ympev.2010.07.005

    Folmer, O., Back, M., Hoeh, W., Lutz, R. & 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.

    Gomes, S.I.L., Novais, S.C., Soares, A.M.V.M. & Amorim, M.J.B. (2011) Effects of soil properties and time of exposure on gene expression of Enchytraeus albidus (Oligochaeta). Soil Biology and Biochemistry, 43, 2078–2084.
    https://doi.org/10.1016/j.soilbio.2011.06.006

    Henle, F.G.J. (1837) Ueber Enchytraeus, eine neue Anneliden-Gattung. Müllers Archiv für Anatomie, Physiologie und wissenschaftliche Medizin, Berlin, 1837, 74–90.

    Hrabě, S. (1935) Oligohety ozera Issyk-Kul. Die Oligochaeten des Issykkulsees. (The oligochaetes of Lake Issyk-Kul. In Russian with German summary.) Akademiya Nauk SSSR, Trudy Kirgizskoj kompleksnoj expedicii, 3, 73–85.

    Kaden, H., Peeters, F., Lorke, A., Kipfer, R., Tomonaga, Y. & Karabiyikoglu, M. (2010) Impact of lake level change on deep-water renewal and oxic conditions in deep saline Lake Van, Turkey. Water Resources Research, 46 (W11508), 1–14.
    https://doi.org/10.1029/2009WR008555

    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
    https://doi.org/10.1093/molbev/mst010

    Kempe, S., Khoo, F. & Guryelik, Y. (1978) Hydrography of Lake Van and its drainage are. In: Degens, E.T. & Kurtman, F. (Eds.), The geology of Lake Van. MTA, Ankara, pp. 30–44.

    Kempe, S. & Degens, E.T. (1978) Varves in The Black Sea and in Lake Van (Turkey). In: Schüchter, C. (Ed.), Moraines and Varves, Proceedings of an Inqua Symposium of Genesis and Lithology of Quaternary Deposits Zurich 10–20 Sept, pp. İ–xiii + 1–441. [printed in 1979]

    Kempe, S., Kazmierczak, J., Landmann, G., Konuk, T., Reimer, A. & Lipp, A. (1991) Largest known microbialites discovered in Lake Van, Turkey. Nature, 349, 605–608.
    https://doi.org/10.1038/349605a0

    Kuperman, R.G., Simini, M., Phillips, C.T. & Checkai, R.T. (1999) Comparison of malathion toxicity using enchytraeid reproduction test and earthworm toxicity test in different soil types. Pedobiologia, 43, 630–634.

    Lanfear, R., Calcott. B., Ho, S.Y. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
    https://doi.org/10.1093/molbev/mss020

    Litt, T., Krastel, S., Sturm, M., Kipfer, R., Orcen, S., Heumann, G., Franz, S.O., Ulgen, U.B. & Niessen, F. (2009) ‘PALEOVAN’, International Continental Scientific Drilling Program (ICDP): site survey results and perspectives. Quaternary Science Reviews, 28,1555–1567.
    https://doi.org/10.1016/j.quascirev.2009.03.002

    López-García, P., Kazmierczak, J., Benzerara, K., Kempe, S., Guyot, F. & Moreira, D. (2005) Bacterial diversity and carbonate precipitation in the giant microbialites from the highly alkaline Lake Van, Turkey. Extremophiles, 9, 263–274.
    https://doi.org/10.1007/s00792-005-0457-0

    Maraldo, K., Weber Ravn, H., Slotsbo, S. & Holmstrup, M. (2009) Responses to acute and chronic desiccation stress in Enchytraeus (Oligochaeta: Enchytraeidae). Comparative Physiology B, 179, 113–123.
    https://doi.org/10.1007/s00360-008-0305-5

    Matamoros, L., Yıldız, S. & Erseus, C. (2007) A new species within the genus Marionina (Enchytraeidae:Annelida:Clitellata) from the southern Black Sea. Marine Biology Research, 3 (6), 397–402.
    https://doi.org/10.1080/17451000701694844

    Mittermeier, R.A., Gil, P.R., Hoffman, M., Pilgrim, J., Brooks, T., Mittermeier, J.C., Lamoreux, J. & da Fonseca, G.A.B. (2005) Hotspots Revisited: Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions. Chicago University Press, Chicago, 392 pp.

    Nielsen, C.O. & Christensen, B. (1959) The Enchytraeidae. Critical revision and taxonomy of European species (Studies on Enchytraeidae VII). Natura Jutlandica, 8–9, 1–160.

    Novais, S.C. & Amorim, M.J.B. (2015) Normal operating range (NOR) in Enchytraeus albidus—Transcriptional responses to control conditions. Applied Soil Ecology, 85, 1–10.
    https://doi.org/10.1016/j.apsoil.2014.08.005

    Novais, S.C., Arrais, J., Lopes, P., Vandenbrouck, T., De Coen, W., Roelofs, D., Soares Amadeu, M.V.M. & Amorim, M. (2012) Enchytraeus albidus microarray: enrichment, design, annotation and database (EnchyBASE). PLoS ONE, 7 (4), e34266. https://doi.org/10.1371/journal.pone.0034266

    Patricio Silva, A.L., Holmstrup, M., Kostal, V. & Amorim, M.J.B. (2013) Soil salinity increases survival of freezing in the enchytraeid Enchytraeus albidus. Journal of Experimental Biology, 216, 2732–2740.
    https://doi.org/10.1242/jeb.083238

    Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21 (8), 1864–1877.
    https://doi.org/10.1111/j.1365-294X.2011.05239.x

    Reemer, M. & Smit, J.T. (2007) Some hoverfly records from Turkey (Diptera, Syrphidae). Volucella, 8, 135–146.

    Reimer, A., Landmann. G. & Kempe, S. (2009) Lake Van, Eastern Anatolia, hydrochemistry and history. Aquatic Geochemistry, 15, 195–222.
    https://doi.org/10.1007/s10498-008-9049-9

    Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, 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

    Rota, E. & Manconi, R. (2004) Taxonomy and ecology of sponge-associate Marionina spp. (Clitellata: Enchytraeidae) from the Horomatangi geothermal system of Lake Taupo, New Zealand. International Revue of Hydrobiology, 89, 58–67.
    https://doi.org/10.1002/iroh.200310695

    Schmelz, R.M. & Collado, R. (2010) A guide to European terrestrial and freshwater species of Enchytraeidae (Oligochaeta). Soil Organisms, 82, 1–176. Available from: http://www.senckenberg.de/root/index.php?page_id=13185 (Acesses 20 Feb. 2018)

    Sperber, C. (1958) Über einige Naididae aus Europa, Asien und Madagaskar. Archiv für Zoologie, 12, 45–53.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
    https://doi.org/10.1093/molbev/mst197

    Timm, T., Arslan, N., Rüzgar, M., Martinsson, S. & Erseus, C. (2013) Oligochaeta (Annelida) of the profundal of Lake Hazar (Turkey), with description of Potamothrix alatus hazaricus n. ssp. Zootaxa, 3716 (2), 144–156.
    https://doi.org/10.11646/zootaxa.3716.2.2

    Yıldız, Ş., Özgökçe, M.S., Özgökçe, F., Karaca, İ. & Polat, E. (2010) Zooplankton composition of Van Lake coastline in Turkey. African Journal of Biotechnology, 9 (48), 8248–8252.
    https://doi.org/10.5897/AJB10.538