Following the Phoenician example: western Mediterranean colonization by Spirobranchus cf. tetraceros (Annelida: Serpulidae)

Authors

DOI:

https://doi.org/10.3989/scimar.04976.20A

Keywords:

cryptic species, ports, shipping, biological invasions, polychaetes, cytochrome b, identification key

Abstract


A newly established population of the fouling polychaete Spirobranchus cf. tetraceros is reported from the western Mediterranean (Valencia Port). Despite previous intensive surveys, this is the first record for the taxon in the Iberian Peninsula. Molecular analyses revealed that S. cf. tetraceros from Valencia are genetically identical to specimens from Heraklion, Crete, but different from those collected in the Red Sea and S. tetraceros sensu stricto from the type locality in Australia. Mediterranean and Red Sea S. cf. tetraceros form a well-supported monophyletic clade but are clearly distinct from New South Wales specimens of S. tetraceros. Our new molecular evidence supports the hypothesis that S. tetraceros is not a global invader of Australian origin but rather a large species complex in need of a comprehensive worldwide revision. These results highlight the importance of integrative taxonomic research for species with reported global distributions because these taxa may include cryptic invaders. An illustrated morphological account of the Valencia and Heraklion specimens and a taxonomic key for Spirobranchus species in the Mediterranean Sea are provided.

Downloads

Download data is not yet available.

References

Antoniadou C., Nicolaidou A., Chintiroglou C. 2004. Polychaetes associated with the sciaphilic alga community in the northern Aegean Sea: Spatial and temporal variability. Helgol. Mar. Res. 58: 168-182. https://doi.org/10.1007/s10152-004-0182-6

Baird W. 1865. Description of several new species and varieties of tubicolous annelides = Tribe LIMIVORA of Grube, in the collection of the British Museum. J. Linn. Soc. Lond. Zool. 8: 10-22. https://doi.org/10.1111/j.1096-3642.1864.tb02002.x

Bastida-Zavala J.R., ten Hove H.A. 2002. Revision of Hydroides Gunnerus, 1768 (Polychaeta: Serpulidae) from the western Atlantic region. Beaufortia 52: 103-178.

Ben-Eliahu M.N. 1991. Red Sea serpulids (Polychaeta) in the eastern Mediterranean. Ophelia Suppl. 5: 515-528.

Ben-Eliahu M.N., ten Hove H.A. 1992. Serpulid tubeworms (Annelida: Polychaeta) a recent expedition along the Mediterranean coast of Israel finds new populations buildups of Lessepsian migrant species. Isr. J. Zool. 38: 35-53.

Ben-Eliahu M.N., ten Hove H.A. 2011. Serpulidae (Annelida: Polychaeta) from the Suez Canal from a Lessepsian migration perspective (a monograph). Zootaxa 2848: 1-147. https://doi.org/10.11646/zootaxa.2848.1.1

Blainville H.M.D. de. 1818. Mémoire sur la classe des Sétipodes, partie des Vers à sang rouge de M. Cuvier, et des Annélides de M. de Lamarck. Bull. Sci. Soc. Philom. Paris 1818: 78-85.

Boore J.L., Brown W.M. 2000. Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol. Biol. Evol. 17: 87-106. https://doi.org/10.1093/oxfordjournals.molbev.a026241 PMid:10666709

Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17: 540-552. https://doi.org/10.1093/oxfordjournals.molbev.a026334 PMid:10742046

Çinar M.E. 2006. Serpulid species (Polychaeta: Serpulidae) from the Levantine coast of Turkey (eastern Mediterranean), with special emphasis on alien species. Aquat. Inv. 1: 223-240. https://doi.org/10.3391/ai.2006.1.4.6

Çinar M.E. 2013. Alien polychaete species worldwide: Current status and their impacts. J. Mar. Biol. Assoc. UK 93: 1257-1278. https://doi.org/10.1017/S0025315412001646

Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797. https://doi.org/10.1093/nar/gkh340 PMid:15034147 PMCid:PMC390337

Fauvel P. 1923. Un nouveau serpulien d'eau saumatre Mercierella n. g., enigmatica n. sp. Bull. Soc. Zool. Fr. 47: 424-430.

Ferrario J., Caronni S., Occhipinti-Ambrogi A., et al. 2017. Role of commercial harbours and recreational marinas in the spread of non-indigenous fouling species. Biofouling 33: 651-660. https://doi.org/10.1080/08927014.2017.1351958 PMid:28786306

Giangrande A., Delos A.L., Musco L., et al. 2004. Polychaete assemblages of rocky shore along the South Adriatic coast (Mediterranean Sea). Cah. Biol. Mar. 45: 85-95.

Glasby T.M., Connell S.D., Holloway M.G., et al. 2007. Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions? Mar. Biol. 151: 887-895. https://doi.org/10.1007/s00227-006-0552-5

Gray E. 1843. Fauna of New Zealand. In: Dieffenbach E., Travels in New Zealand. vol. 2: 30-138, John Murray, London.

Grube A.E. 1862. Mittheilungen über die Serpulen, mit besonderer Berücksichtigung ihrer Deckel. Jahresber. Abh. Schles. Ges. Breslau 39: 53-69.

Gunnerus J.E. 1768. Om Nogle Norske Coraller. Kongel. Norske Vidensk. Selsk. Skr. 4: 38-73.

Haswell W.A. 1883. On some new Australian tubicolous annelids. Proc. Linn. Soc. N.S.W. 7: 633-638.

Kumar S., Stecher G., Li M., et al. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 35: 1547-1549. https://doi.org/10.1093/molbev/msy096 PMid:29722887 PMCid:PMC5967553

Laubier L. 1966. Sur quelques Annélides Polychètes de la région de Beyrouth. Am. Univ. Beirut Misc. Pap. 5: 9-22.

Linnaeus C. von. 1758. Systema Naturae, 10th edition, Vol. 1. L. Salvius, Holmiae, 823 pp.

López E., Richter A. 2017. Non-indigenous species (NIS) of polychaetes (Annelida: Polychaeta) from the Atlantic and Mediterranean coasts of the Iberian Peninsula: an annotated checklist. Helgol. Mar. Res. 71: 19. https://doi.org/10.1186/s10152-017-0499-6

Marenzeller E. von. 1885. Südjapanische Anneliden. II. Ampharetea, Terebellacea, Sabellacea, Serpulacea. Denkschriften der Akademie der Wissenschaften, Wien 49: 197-224.

Megina C., González-Duarte M.M., López-González P.J., et al. 2013. Harbours as marine habitats: Hydroid assemblages on sea-walls compared with natural habitats. Mar. Biol. 160: 371-381. https://doi.org/10.1007/s00227-012-2094-3

Megina C., González-Duarte M.M., López-González P.J. 2016. Benthic assemblages, biodiversity and invasiveness in marinas and commercial harbours: an investigation using a bioindicator group. Biofouling 32: 465-475. https://doi.org/10.1080/08927014.2016.1151500 PMid:26960078

Mineur F., Cook E.J., Minchin D., et al. 2012. Changing coasts: marine aliens and artificial structures. Oceanogr. Mar. Biol. 50: 189-234. https://doi.org/10.1201/b12157-5

Morais P., Reichard M. 2018. Cryptic invasions: a review. Sci. Total Environ. 613-614: 1438-1448. https://doi.org/10.1016/j.scitotenv.2017.06.133 PMid:28648374

Mörch O.A.L. 1863. Revisio critica Serpulidarum. Et Bidrag til Rørormenes Naturhistorie. Naturh. Tidsskr. København, Ser. 3, 1: 347-470.

Pallas P.S. 1766. Miscellanea Zoologica. Petrum van Cleef. Hagae Comitum, The Hague, 224 pp.

Palero F., Hall S., Clark P.F., et al. 2010. DNA extraction from formalin-fixed tissue: new light from the Deep-Sea. Sci. Mar. 74: 465-470. https://doi.org/10.3989/scimar.2010.74n3465

Perry O., Bronstein O., Simon-Blecher N., et al. 2018. On the genus Spirobranchus (Annelida, Serpulidae) from the northern Red Sea, and a description of a new species. Invertebr. Syst. 32: 605-625. https://doi.org/10.1071/IS17061

Philippi A. 1844. Einige Bemerkungen über die Gattung Serpula, nebst Aufzählung der von mir im Mittelmeer mit dem Thier beobachteten Arten. Arch. Naturgesch. 10: 186-198. https://doi.org/10.5962/bhl.part.29558

Quatrefages A. de. 1866. Histoire naturelle des Annelés marins et d'eau douce. Annélides et Géphyriens. Librarie Encyclopédique de Roret. Paris. Vol. 1. 1-588 https://doi.org/10.5962/bhl.title.122818

Read G., Fauchald K. (ed.). 2019. World Polychaeta database. Accessed on 19/10/2019.

Rouse G.W. 2000. Family Serpulidae. In: Beesley P.L., Ross G.L.B., Glasby C.J. (ed.), Polychaetes and Allies: The Southern Synthesis, CSIRO. Melbourne. pp. 184-189.

Schmarda L.K. 1861. Neue Wirbellose Thiere: Beobachted und Gesammelt auf einer Reise um die Erdr 1853 bis 1857. In: Turbellarien, Rotatorien und Anneliden. Leipzig, Verlag von Wilhelm Engelmann. Erster Band, Zweite Hälfte.

Simon C.A., van Niekerk H.H., Burghardt I., et al. 2019. Not out of Africa: Spirobranchus kraussii (Baird, 1865) is not a global fouling and invasive serpulid of Indo-Pacific origin. Aquat. Inv. 14: 221-249. https://doi.org/10.3391/ai.2019.14.2.05

Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313. https://doi.org/10.1093/bioinformatics/btu033 PMid:24451623 PMCid:PMC3998144

Streftaris N., Zenetos A. 2006. Alien marine species in the Mediterranean - the 100 "worst invasives" and their impact. Mediterr. Mar. Sci. 7: 87-118. https://doi.org/10.12681/mms.180

Talavera G., Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56: 564-577. https://doi.org/10.1080/10635150701472164 PMid:17654362

ten Hove H.A. 1970. Serpulinae (Polychaeta) from the Caribbean: I - The genus Spirobranchus. Stud. Fauna Curaçao Caribb. Isl. 32: 1-57.

ten Hove H.A., Kupriyanova E.K. 2009. Taxonomy of Serpulidae (Annelida, Polychaeta): The state of affairs. Zootaxa 2036: 1-126. https://doi.org/10.11646/zootaxa.2036.1.1

Tyrrel M.C., Byers J. 2007. Do artificial substrates favor nonindigenous fouling species over native species? J. Exp. Mar. Biol. Ecol. 342: 54-60. https://doi.org/10.1016/j.jembe.2006.10.014

Ulman A., Ferrario J., Occhpinti-Ambrogi A., et al. 2017. A massive update of non-indigenous species records in Mediterranean marinas. PeerJ 5: e3954. https://doi.org/10.7717/peerj.3954 PMid:29085752 PMCid:PMC5659216

Ulman A., Ferrario J., Forcada A., et al. 2019a. A hitchhiker's guide to alien species settlement in Mediterranean marinas. J. Environ. Manage. 241: 328-339. https://doi.org/10.1016/j.jenvman.2019.04.011 PMid:31015083

Ulman A., Ferrario J., Forcada A., et al. 2019b. Alien species spreading via biofouling on recreational vessels in the Mediterranean Sea. J. Appl. Ecol. 56: 2620-2629. https://doi.org/10.1111/1365-2664.13502

Willette D.A., Iñiguez A.R., Kupriyanova E.K., et al. 2015. Christmas tree worms of Indo-Pacific coral reefs: untangling the Spirobranchus corniculatus (Grube, 1862) complex. Coral Reefs 34: 899-904. https://doi.org/10.1007/s00338-015-1294-y

Zenetos A., Gofas S., Verlaque M., et al. 2010. Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union's Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Mediterr. Mar. Sci. 11: 381-493.

Zenetos A., Çinar M.E., Crocetta F., et al. 2017. Uncertainties and validation of alien species catalogues: The Mediterranean as an example. Estuar. Coast. Shelf Sci. 191: 171-187. https://doi.org/10.1016/j.ecss.2017.03.031

Zibrowius H. 1979. Serpulidae (Annélida Polychaeta) de l'Océan Indien arrivés sur le côques de bateaux à Toulon (France, Méditerranée). Rapp. P.-V. Reun. Comm. Int. Explor. Sci. Mer Mediterr. 25-26: 133-134.

Published

2020-03-30

How to Cite

1.
Palero F, Torrado H, Perry O, Kupriyanova E, Ulman A, Genis-Armero R, ten Hove HA, Capaccioni-Azzati R. Following the Phoenician example: western Mediterranean colonization by Spirobranchus cf. tetraceros (Annelida: Serpulidae). Sci. mar. [Internet]. 2020Mar.30 [cited 2024Mar.28];84(1):83-92. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1846

Issue

Section

Articles

Most read articles by the same author(s)