Abstract
New data from barcode index numbers (BINs) and 28S rRNA gene sequences confirm a cryptic species pair in Lyrodus pedicellatus from the eastern Mediterranean and European Atlantic coasts. Therefore, it is paramount to associate the new species to a scientific name for a reliable reference system of biological information. To this end, we describe Lyrodus mersinensis sp. nov., another cryptic species in the L. pedicellatus complex, and redescribe the `true´ L. pedicellatus. Both the description and redescription are based on molecular diagnostic characters obtained from sequences of the mitochondrial cytochrome c oxidase subunit I (COI) and nuclear 28S rRNA genes. The 18S rRNA gene sequences did not yield diagnostic characters to distinguish these species. A morphological diagnosis of pedicellatus-like Lyrodus species is also provided.
References
Bartsch, P. (1916) A New Teredo from the west coast of America. Nautilus, 30 (4), 47–48.
Bartsch, P. (1921) A new classification of the shipworms and descriptions of some new wood boring mollusks. Proceedings of the Biological Society of Washington, 35, 25–32.
Bartsch, P. (1922) A Monograph of the American shipworms. Bulletin of the United States national Museum, 122, 1–48.
https://doi.org/10.5479/si.03629236.122.iBartsch, P. (1927) New species of shipworm from Siam. Journal of the Siam Society, Natural History, Supplement 7 (1), 59–63.
Bartsch, P. (1927) The shipworms of the Philippine Islands. Bulletin of the United States national Museum, 100, 2 (5), 553–562.
Bauer, A.M., Parham, J.F., Brown, R.M., Stuart, B.L., Grismer, L., Papenfuss, T.J., Böhme, W., Savage, J.M., Carranza, S., Grismer, J.L., Wagner, P., Schmitz, A., Ananjeva, N.B. & Inger, R.F. (2011) Availability of new Bayesian-delimited gecko names and the importance of character-based species descriptions. Proceedings. Biological Sciences, The Royal Society, 278, 490–492.
https://doi.org/10.1098/rspb.2010.1330Bergmann, T., Hadrys, H. & Breves, G. (2009) Character-based DNA barcoding: a superior tool for species classification. Berliner und Münchener tierärztliche Wochenschrift, 122 (11–12), 446–450.
https://doi.org/10.2376/0005-9366-122-446Borges, L.M.S. (2014) Biodegradation of wood exposed in the marine environment: Evaluation of the hazard posed by marine wood-borers in fifteen European sites. International Biodeterioration and Biodegradation, 96, 97–104.
https://doi.org/10.1016/j.ibiod.2014.10.003Borges, L.M.S. (2016) The internal structure of the pallets of Nototeredo norvagica and Psiloteredo megotara (Bivalvia: Teredinidae): implications for subfamilial allocations. Zoomorphology, 135 (1), 33–41.
https://doi.org/10.1007/s00435-015-0277-4Borges, L.M.S., Merckelbach, L.M., Sampaio, I. & Cragg, S.M. (2014a) Diversity, environmental requirements, and biogeography of bivalve wood-borers (Teredinidae) in European coastal waters. Frontiers in Zoology, 11, 13.
https://doi.org/10.1186/1742-9994-11-13Borges, L.M.S., Merckelbach, L.M. & Cragg, S.M. (2014b) Biogeography of wood-boring crustaceans (Isopoda: Limnoriidae) established in European Coastal waters. Public Library of Science ONE, 9 (10), e109593.
https://doi.org/10.1371/journal.pone.0109593Borges, L.M.S., Sivrikaya, H., Le Roux, A., Shipway, J.R., Cragg, S.M. & Costa, F.O. (2012) Investigating the taxonomy and systematics of marine wood borers (Bivalvia: Teredinidae) combining evidence from morphology, DNA barcodes and nuclear locus sequences. Invertebrate Systematics, 26, 572–582.
https://doi.org/10.1071/IS12028Calloway, C.B. & Turner, R.D. (1983) Documentation and implications of rapid successive gametogenic cycles and broods in the shipworm Lyrodus floridanus (Bartsch) (Bivalvia, Teredinidae). Journal of Shellfish Research, 3, 65–69.
Calloway, C.B. & Turner, R.D. (1988) Brooding in the Teredinidae (Mollusca: Bivalvia). In: Thomson, M.-F., Sarojini, R. & Nagabhushanam, R. (Eds.), Marine Biodeterioration. Oxford & IBH Publishing Company, Goa, pp. 215–226.
Carlton, J.T. & Hodder, J. (1995) Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th-century sailing vessel. Marine Biology, 121, 721–730.
https://doi.org/10.1007/bf00349308Carlton, J.T. (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanography and Marine Biology, 23, 313–371.
Carlton, J.T. (1999) Molluscan invasions in marine and estuarine communities. Malacologia, 41, 439–454.
Carlton, J.T., Chapman, J.W., Geller, J.B., Miller, J.A., Carlton, D.A., McCuller, M.I., Treneman, N.C., Steves, B.P. & Ruiz, G.M. (2017) Tsunami-driven rafting: Transoceanic species dispersal and implications for marine biogeography. Science, 357 (6358), 1402–1406.
https://doi.org/10.1126/SCIENCE.AAO1498Chessman, B., Williams, S. & Besley, C. (2007) Bioassessment of streams with macroinvertebrates: effect of sampled habitat and taxonomic resolution. Journal of the North American Benthological Society, 26 (3), 546–565.
https://doi.org/10.1899/06-074.1
Chiarucci, A., Bacaro, G. & Scheiner, S. (2011) Old and new challenges in using species diversity for assessing biodiversity. Phylosophical Transactions of the Royal Society B: Biological Sciences, 366 (1756), 2426–2437.
https://doi.org/10.1098/rstb.2011.0065Cook, L.G., Edwards, R.D., Crisp, M.D. & Hardy, N.B. (2010) Need morphology always be required for new species descriptions? Invertebrate Systematics, 24 (3), 322–326.
https://doi.org/10.1071/IS10011Costa, F.O. & Antunes, P.M. (2012) The Contribution of the Barcode of Life Initiative to the Discovery and Monitoring of Biodiversity. In: Mendonça, A., Cunha, A. & Ranjan, C. (Eds.), Natural Resources, Sustainability and Humanity. Springer, Dordrecht, pp. 37–68.
https://doi.org/10.1007/978-94-007-1321-5_4Dall, W.H., Bartsch, P. & Rehder, H.A. (1938) A manual of the recent and fossil marine pelecypod mollusks of the Hawaiian Islands. Bernice P. Bishops Museum Bulletin, Honolulu, 153, 1–253.
De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56 (6), 879–886.
https://doi.org/10.1080/10635150701701083DeSalle, R., Egan, M.G. & Siddall, M. (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 360 (1462), 1905–1916.
https://doi.org/10.1098/rstb.2005.1722Distel, D.L., Amin, M., Burgoyne, A., Linton, E., Mamangkey, G., Morrill, W., Nove, J., Wood, N. & Yang, J. (2011) Molecular phylogeny of Pholadoidea Lamarck, 1809 supports a single origin for xylotrophy (wood feeding) and xylotrophic bacterial endosymbiosis in Bivalvia. Molecular Phylogenetics and Evolution, 61 (2), 245–254.
https://doi.org/10.1016/j.ympev.2011.05.019Edgar, 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/gkh340Edmondson, C.H. (1946) Dispersal of shipworms among Central Pacific islands, with the description of new species. Occasional papers of the Bernice P. Bishop Museum, Honolulu, 18 (15), 211–224.
Félix, M.A., Braendle, C. & Cutter, A.D. (2014) A streamlined system for species diagnosis in Caenorhabditis (Nematoda: Rhabditidae) with name designations for 15 distinct biological species. Public Library of Science ONE, 9 (4), e0118327.
https://doi.org/10.1371/journal.pone.0094723Gollasch, S. (2002) The importance of ship hull fouling as a vector of species introductions into the North Sea. Biofouling, 18 (2), 105–121.
https://doi.org/10.1080/08927010290011361Gould, A.A. (1870) Report on the invertebrata of Massachusetts. Wright and Potter, State Printers, Boston, 524 pp.
https://doi.org/10.5962/bhl.title.10312Gray, J.E. (1827) A monograph of the genus Teredo of Linné, with descriptive characters of the species in the British Museum. Philosophical Magazine (London), 2 (12), 409–411.
https://doi.org/10.1080/14786442708674441Harvey, R. (1996) Deep water Xylophagaidae (Pelecypoda: Pholadacea) from the North Atlantic with description of three new species. Journal of Conchology, 35, 473–481.
Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences, 270 (1512), 313–321.
https://doi.org/10.1098/rspb.2002.2218Hebert, 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 of the United States of America, 101 (41), 14812–14817.
https://doi.org/10.1073/pnas.0406166101Hebert, P.D.N., Ratnasingham, S. & de Waard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B: Biological Sciences, 270 (Supplement 1), 96–99. [S96–S99]
https://doi.org/10.1098/rsbl.2003.0025Hoagland, K.E. & Turner, R.D. (1981) Evolution and adaptative radiation of wood-boring bivalves (Pholadacea). Malacologia, 21, 11–148.
International Commission on Zoological Nomenclature (1999) International code of zoological nomenclature. Fourth edition. International Trust for Zoological Nomenclature, London, xxix + 306 pp.
https://doi.org/10.5962/bhl.title.50608Iredale, T. (1932) Cobra or shipworms: a systematic account of the teredinid molluscs of Port Jackson. In: Iredale, T. (Ed.), Destruction of timber by marine organisms in the port of Sydney. Sydney Harbour Trust, Sydney, pp. 24–40.
Iredale, T. (1936) Queensland cobra or shipworms: a systematic account of the teredinid molluscs of South Queensland. In: Watson, C.J.J. (Ed.), Destruction of timber by marine organisms in the Port of Brisbane Bulletin 12. Queensland Forest Service, Queensland, pp. 31–44.
Jörger, K.M. & Schrödl, M. (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology, 10, 59.
https://doi.org/10.1186/1742-9994-10-59Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, 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/bts199Kizirian, D. & Donnelly, M.A. (2004) The criterion of reciprocal monophyly and classification of nested diversity at the species level. Molecular Phylogenetics and Evolution, 32 (3), 1072–1076.
https://doi.org/10.1016/j.ympev.2004.05.001Knowlton, N. (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia, 420, 73–90.
https://doi.org/10.1023/A:1003933603879Kuronuma, K. (1931) On the Japanese ship-worms, with description of three new species. Venus, Kyoto, 2 (6), 294–304.
Lamy, É. (1923) Les tarets de la Mer Rouge (d´aprés les materiaux recueillis par le Dr Jousseaume). Bulletin du Muséum national d´Histoire naturelle, Paris, 29 (2), 175–178. [in French]
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., Mcgettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23 (21), 2947–2948.
https://doi.org/10.1093/bioinformatics/btm404Lebour, M.V. (1946) The species of Teredo from Plymouth waters. Journal of the Marine Biological Association of the United Kingdom, 26, 381–389.
https://doi.org/10.1017/s0025315400012200Lenat, D.R. & Resh, V.H. ( 2001) Taxonomy and stream ecology–The benefits of genus- and species-level identifications. Journal of the North American Benthological Society, 20 (2), 287–298.
https://doi.org/10.2307/1468323Linnaeus, C. (1758) Systemae Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio decima, reformata. Laurentius Salvius: Holmiae, Stockholm, 823 pp. [in Latin]
Macintosh, H. (2012) Lyrodus turnerae, a new teredinid from eastern Australia and the Coral Sea (Bivalvia: Teredinidae). Molluscan Research, 32 (1), 36–42.
Miller, R.C. (1924) Wood-boring mollusks from the Hawaiian, Samoan and Philippine Islands. University of California Publications in Zoology, 26 (7), 145–158.
Miranda, L. & Thiel, M. (2008) Active and passive migration in boring isopods Limnoria spp. (Crustacea, Peracarida) from kelp holdfasts. Journal of Sea Research, 60 (3), 176–183.
https://doi.org/10.1016/j.seares.2008.06.002Moll, F. (1936) Über Wanderungen von Terediniden. Mitteilungen der Gesellschaft für Vorratsschutz, 12 (1), 3–4. [in German]
Moll, F. (1941) Übersicht über die Terediniden des Museums für Naturkunde zu Berlin. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, 1941, 152–225. [in German]
Moll, F. & Roch, F. (1931) The Teredinidae of the British Museums, the natural history museums in Glasgow and Manchester, and the Jeffreys collection. Journal of Molluscan Studies, 19 (4), 201–218.
https://doi.org/10.1093/oxfordjournals.mollus.a064041Nair, N.B. (1956) Shipworms from India. I. Report on ten species of shipworms from the Madras coast. Records of the Indian Museum, 52, 387–414.
Nair, N.B. (1958) Shipworms of India. II. Seven more shipworms from South India. Records of the Indian Museum, 53, 261–278.
Pechenik, J.A., Perron, F.E. & Turner, R.D. (1979) The role of phytoplankton in the diets of adult and larval shipworms, Lyrodus pedicellatus (Bivalvia: Teredinidae). Estuaries and Coasts, 2 (1), 58–60.
https://doi.org/10.2307/1352042Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D., Vogler, A.P. & Hedin, M. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55 (4), 595–609.
https://doi.org/10.1080/10635150600852011Puillandre, N., Modica, M.V., Zhang, Y., Sirovich, L., Boisselier, M.C., Cruaud, C., Holford, M. & Samadi, S. (2012) Large-scale species delimitation method for hyperdiverse groups. Molecular Ecology, 21 (11), 2671–2691.
https://doi.org/10.1111/j.1365-294X.2012.05559.xQuatrefages, A. (1849) Mémoire sur le genre Taret (Teredo Linn.). Annales des Sciences Naturelles, Zoologique, 11, 19–64. [in French]
Rach, J., DeSalle, R., Sarkar, I.N., Schierwater, B. & Hadrys, H. (2008) Character-based DNA barcoding allows discrimination of genera, species and populations in Odonata. Proceedings of the Royal Society B: Biological Sciences, 275 (1632), 237–247.
https://doi.org/10.1098/rspb.2007.1290Radulovici, A.E., Archambault, P. & Dufresne, F. (2010) DNA barcodes for marine biodiversity: Moving fast forward? Diversity, 2 (4), 450–472.
https://doi.org/10.3390/d2040450Ratnasingham, S. & Hebert, P.D.N. (2007) BARCODING, BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes, 7, 355–364.
https://doi.org/10.1111/j.1471-8286.2006.01678.xRatnasingham, S. & Hebert, P.D.N. (2013) A DNA-Based Registry for All Animal Species: The Barcode Index Number (BIN) System. Public Library of Science ONE, 8 (7), e66213.
https://doi.org/10.1371/journal.pone.0066213Raupach, M., Astrin, J., Hannig, K., Peters, M., Stoeckle, M. & Wagele, J.-W. (2010) Molecular species identification of Central European ground beetles (Coleoptera: Carabidae) using nuclear rDNA expansion segments and DNA barcodes. Frontiers in Zoology, 7, 26.
https://doi.org/10.1186/1742-9994-7-26Renner, S.S. (2016) A Return to Linnaeus’s Focus on Diagnosis, Not Description: The Use of DNA Characters in the Formal Naming of Species. Systematic Biology, 65 (6), 1085–1095.
https://doi.org/10.1093/sysbio/syw032Roch, F. (1931) Die Terediniden der skandinavischen Mueseumssammlungen (Stockholm, Gothenburg, Kopenhagen, Oslo, Nidaros und Tromsø). Arkiv för Zoologi, 22, 1–29. [in German]
Roch, F. & Moll, F. (1929) Die Terediniden der Zoologischen Museen zu Berlin und Hamburg. Mitteilungen aus dem Zoologischen Staatsinstitut und Zoologischen Museum in Hamburg, 44, 1–22. [in German]
Roch, F. & Moll, F. (1935) Über einige neue Teredinidenarten. Sitzungsberichte, Akademie der Wissenschaften in Wien, Mathematish-naturwissenschaftliche Klasse I, Biologie, Mineralogie, Erdkunde, Abt. 1, 144 (5–6), 263–279. [in German]
Romano, C., Voight, J.R., Pérez-Portela, R., & Martin, D. (2014) Morphological and genetic diversity of the wood-boring Xylophaga (Mollusca, Bivalvia): New species and records from deep-sea Iberian canyons. Public Library of Science ONE, 9 (7), e102887.
https://doi.org/10.1371/journal.pone.0102887Sanders, M.T., Merle, D., Bouchet, P., Castelin, M., Beu, A.G., Samadi, S. & Puillandre, N. (2017) One for each ocean: revision of the Bursa granularis (Röding, 1798) species complex (Gastropoda: Tonnoidea: Bursidae). Journal of Molluscan Studies, 83 (4), 384–398.
https://doi.org/10.1093/mollus/eyx029Spengler, L. (1792) Betragtninger og Anmaerkniger ved den Linneiske Slaegt Pholas blantde mangeskallede Muskeler, med dens hidindtil bekiendte gamle og nye Arter, samt den dermed i Forbindelse staaende Slaegt Teredo Linn. Skrivter af Naturhistorie- Selskabet (Kiøenhavn), 2 (1), 72–106. [in Danish]
Taki, I. & Habe, T. (1945) On the teredinid species of Ambon and Nicobar. Kairuigaku zasshi, Oshima, 14 (1–4), 118–123.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30 (12), 2725–2729.
https://doi.org/10.1093/molbev/mst197Taylor, J., Williams, S.T., Glover, E.A. & Dyal, P. (2007) A molecular phylogeny of heterodont bivalves (Mollusca: Bivalvia: Heterodonta): New analyses of 18S and 28S rRNA genes. Zoologica Scripta, 36 (6), 587–606.
https://doi:10.1111/j.1463-6409.2007.00299.xTreneman, N.C., Borges, L.M.S., Shipway, J.R., Raupach, M.J., Altermark, B. & Carlton, J.T. (2018) A molecular phylogeny of marine-borers (Teredinidae) from Japanese Tsunami Marine Debris. Aquatic Invasions, 23 (1), 101–112.
https://doi.org/10.3391/ai.2018.13.1.08Turgeon, D.D., Lyons, W.G., Mikkelsen, P., Rosenberg, G. & Moretzson, F. (2009) Bivalvia (Mollusca) of the Gulf of Mexico. In: Felder, D.K. & Camp, D.L. (Eds.), Gulf of Mexico origin, waters, and biota. A & M University Press, College Station, Texas, pp. 711–744.
Turner, R.D. (1966) A survey and illustrated catalogue of the Teredinidae. The Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts, 265 pp.
https://doi.org/10.5962/bhl.title.67017Turner, R.D. (1971) Identification of marine wood-boring molluscs. In: Jones, E.B.G. & Eltringham, S.K. (Eds.), Marine borers, fungi and fouling organisms. Organisation for Economic Cooperation and Development-OECD, Paris, pp. 17–62.
Voight, J.R. (2015) Xylotrophic bivalves: Aspects of their biology and the impacts of humans. Journal of Molluscan Studies, 81 (2), 175–182.
https://doi.org/10.1093/mollus/eyv008Wang, Y., Zhou, Q.-S., Qiao, H.-J., Zhang, A.-B., Yu, F., Wang, X.-B., Zhu, C.-D. & Zhang, Y.-Z. (2016) Formal nomenclature and description of cryptic species of the Encyrtus sasakii complex (Hymenoptera: Encyrtidae). Scientific Reports, 6, 34372.
https://doi.org/10.1038/srep34372Weigelt, R., Lippert, H., Borges, L.M.S., Appelqvist, C., Karsten, U. & Bastrop, R. (2016) First time DNA barcoding of the common shipworm Teredo navalis Linnaeus 1758 (Mollusca: Bivalvia: Teredinidae): Molecular-taxonomic investigation and identification of a widespread wood-borer. Journal of Experimental Marine Biology and Ecology, 475, 154–162.
https://doi.org/10.1016/j.jembe.2015.11.008