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Worming its way into Patagonia: an integrative approach reveals the cryptic invasion by Eulalia clavigera (Annelida: Phyllodocidae)

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Abstract

A phyllodocid polychaete belonging to the genus Eulalia is reported from Nuevo Gulf, Patagonia (South-western Atlantic Ocean) with abundant populations thriving in the intertidal zone. Morphological and molecular data allowed assigning this population to Eulalia clavigera (Audouin & Milne-Edwards, 1834), a species typically occurring along the north-eastern Atlantic coast. The absence of genetic structuring between north-eastern and south-western Atlantic E. clavigera strongly supports a non-native origin of the Patagonian population. Conversely, the majority of the Mediterranean Eulalia cf. clavigera analysed in this study turned out to belong to a different, probably undescribed species, suggesting that the diversity and taxonomy of green Eulalia is more complex than previously supposed. The high adaptation capabilities to stressed environments showed by E. clavigera, along with its possible high impact on native assemblages through predation, compel to carefully monitor its spread along the Patagonian coasts.

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References

  • Alós C (2004) Familia Phyllodocidae Örsted, 1843. In: Vieitez JM, Alós C, Parapar J, Besteiro C, Moreira J, Nüñez J, Laborda J, San Martín G (eds) Fauna Iberica 25, Annelida Polychaeta I. Museo Nacional de Ciencias Naturales. CSIC, Madrid, pp 105–209

    Google Scholar 

  • Audouin JV, Milne-Edwards H (1834) Recherches pour servir a l’histoire naturelle du littoral de la France, ou, Recueil de mémoires sur l’anatomie, la physiologie, la classification et les moeurs des animaux des nos côtes: ouvrage accompagné de planches faites d'après nature. volumen 2, Annélides, première partie. Crochard, Paris, 290 pp, 18 pls

  • Barroso R, Klautau M, Solé-Cava AM, Paiva PC (2010) Eurythoe complanata (Polychaeta: Amphinomidae), the ‘cosmopolitan’ fireworm, consists of at least three cryptic species. Mar Biol 157:69–80

    Article  Google Scholar 

  • Bertocci I, Badalamenti F, Lo Brutto S, Mikac B, Pipitone C, Schimmenti E, Vega Fernández T, Musco L (2017) Reducing the data-deficiency of threatened European habitats: spatial variation of sabellariid worm reefs and associated fauna in the Sicily Channel, Mediterranean Sea. Mar Environ Res 130:325–337

    Article  CAS  PubMed  Google Scholar 

  • Blakeslee AM, Byers JE, Lesser MP (2008) Solving cryptogenic histories using host and parasite molecular genetics: the resolution of Littorina littorea’s north American origin. Mol Ecol 17:3684–3696

    Article  CAS  PubMed  Google Scholar 

  • Blank M, Laine AO, Jürss K, Bastrop R (2008) Molecular identification key based on PCR/RFLP for three polychaete sibling species of the genus Marenzelleria, and the species’ current distribution in the Baltic Sea. Helgoland Mar Res 62:129–141

  • Bolton JJ, Andreakis N, Anderson RJ (2011) Molecular evidence for three separate cryptic introduction of the red seaweed Asparagopsis (Bonnemaisoniales, Rhodophyta) in South Africa. Afr J Mar Sci 33:263–271

    Article  Google Scholar 

  • Bonse S, Schmidt H, Eibye-Jacobsen D, Westheide W (1996) Eulalia viridis (Polychaeta: Phyllodocidae) is a complex of two species in northern Europe: results from biochemical and morphological analysis. Cah Biol Mar 37:33–48

    Google Scholar 

  • Borja A, Galparsoro I, Solaun O, Muxika I, Tello EM, Uriarte A, Valencia V (2005) The European water framework directive and the DPSIR, a methodological approach to assess the risk of failing to achieve good ecological status. Estuar Coast Shelf Sci 66:84–96

    Article  Google Scholar 

  • Carlton JT (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conserv Biol 3:265–273

    Article  Google Scholar 

  • Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77:1653–1655

    Article  Google Scholar 

  • Carr CM, Hardy SM, Brown TM, Macdonald TA, Hebert PDN (2011) A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. Plos One 6:e22232

  • Carrera-Parra LF, Salazar-Vallejo SI (2011) Redescriptions of Eunice filamentosa and E. denticulata and description of E. tovarae n. sp. (Polychaeta: Eunicidae), highlighted with morphological and molecular data. Zootaxa 2880:51–64

    Article  Google Scholar 

  • Çinar ME (2013) Alien polychaete species worldwide: current status and their impacts. J Mar Biol Assoc UK 93:1257–1278

    Article  Google Scholar 

  • Çinar ME, Altun C (2007) A preliminary study on the population characteristics of the lessepsian species Pseudonereis anomala (Polychaeta: Nereididae) in Iskenderun Bay (Levantine Sea, eastern Mediterranean). Turk J Zool 31:403–410

    Google Scholar 

  • Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166

    Article  Google Scholar 

  • D’Alessandro M, Romeo T, Castriota L, Cosentino A, Perzia P, Martins R (2016) New records of Lumbrineridae (Annelida: Polychaeta) in the Mediterranean biogeographic province, with an updated taxonomic key. Ital J Zool 83:233–243

    Article  Google Scholar 

  • Ehlers E (1901) Die Polychaeten des magellanischen und chilenischen Strandes: Ein faunisticher Versuch. Fetschrift zur Feier des 150-jährigen Bestehens der Königlichen Gesellschaft der Wissenschaften zu Göttingen. Weidmannsche Buchhandlung, Berlin, 232 pp

  • Emson RH (1977) The feeding and consequent role of Eulalia viridis (O.F. Müller) (Polychaeta) in intertidal communities. J Mar Biol Assoc UK 57:93–96

    Article  Google Scholar 

  • Evans RG (1949) The intertidal ecology of rocky shores in south Pembrokeshire. J Ecol 37:120–139

    Article  Google Scholar 

  • Faulwetter S, Vasileiadou A, Papageorgiou N, Arvanitidis C (2008) Description of a new species of Streptosyllis (Polychaeta: Syllidae) from the Mediterranean and Canary Islands with a re-description of Streptosyllis arenae and comments on the taxonomy of Streptosyllis and some morphologically similar genera. Zootaxa 1847:1–18

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 4:783–791

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Giangrande A (2003) Biodiversity, conservation and the ‘taxonomic impediment’. Aquat Conserv 13:451–459

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp Ser 41:95–98

    CAS  Google Scholar 

  • Holloway MG, Keough MJ (2002) Effects of an introduced polychaete, Sabella spallanzanii, on the development of epifaunal assemblages. Mar Ecol Prog Ser 236:137–154

    Article  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Jeschke JM, Bacher S, Blackburn TM, Dick JTA, Essl F, Evans T, Gaertner M, Hulme PE, Kühn I, Mrugała A, Pergl J, Pyšek P, Rabitsch W, Ricciardi A, Richardson DM, Sendek A, Vilà M, Winter M, Kumschick S (2014) Defining the impact of non-native species. Conserv Biol 28:1188–1194

    Article  PubMed  PubMed Central  Google Scholar 

  • Kato T, Pleijel F, Mawatari SF (2001) Eulalia gemina (Phyllodocidae: Polychaeta), a new species form Shirahama. Jpn Proc Biol Soc Wash 114:381–388

    Google Scholar 

  • Kensler CB (1967) Desiccation resistance of intertidal crevice species as a factor in their zonation. J Anim Ecol 36:391–406

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kinberg JGH (1866) Annulata nova (Nephthydea, Phyllodocea, Alciopea, Hesionida, Glycerea, Goniadea, Syllidea, Ariciea, Spiodea, Aonidea, Cirratulida, Opheliacea). Kongelige Vetenskaps-Akademiens Förhandlingar 22:239–258

    Google Scholar 

  • Kinberg JGH (1910) Konglia Svenska Fregatten Eugenies Resa imkring jorden under befall af C.A. Virgin åren 1851–1853. Vetenskapliga Iakttagelser På H. Maj: T. Konnung Oscar den Förstes befallning utgifna. Kongelige Svenska Vetenskaps-Akademien. Zoologie, 3. Annulata 2:33–78

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:947–2948

    Article  CAS  Google Scholar 

  • Leppäkoski E, Gollasch S, Olenin S (2002) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer Academic Publishers, Dordrecht, p 583

    Book  Google Scholar 

  • Lobo J, Teixeira MAL, Borges LMS, Ferreira MSG, Hollatz C, Gomes PT, Sousa R, Ravara A, Costa MH, Costa FO (2016) Starting a DNA barcode reference library for shallow water polychaetes from the southern European Atlantic coast. Mol Ecol Res 16:298–313

    Article  CAS  Google Scholar 

  • Lodge DM, Williams S, McIsaac HJ, Hayes KR, Leung B, Reichard S, Mack RN, Moyle PB, Smith M, Andow DA, Carlton JT, McMichael A (2006) Biological invasions: recommendations for U.S. policy and management. Ecol Appl 16:2035–2054

    Article  PubMed  Google Scholar 

  • Marchini A, Galil BS, Occhipinti-Ambrogi A (2015) Recommendations on standardizing lists of marine alien species: lessons from the Mediterranean Sea. Mar Pollut Bull 101:267–273

    Article  CAS  PubMed  Google Scholar 

  • Michel C (1970) Role physiologique de la trompe chez quatre annelides polychètes appartenant aux genres: Eulalia, Phyllodoce, Glycera et Notomastus. Cah Biol Mar 11:209–228

    Google Scholar 

  • Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Fr Ecol Environ 6:485–492

    Article  Google Scholar 

  • Morgado EH, Amaral ACZ (1984) Anelídeos poliquetos asociados ao briozário Schizoporella unicornis (Johnston), 4. Phyllodocidae e Hesionidae. Rev Bras Zool 2:49–54

    Article  Google Scholar 

  • Morton B (2011) Predator-prey-scavenging interactions between Nucella lapillus, Carcinus maenas and Eulalia viridis all exploiting Mytilus galloprovincialis on a rocky shore recovering from tributyl-tin (TBT) pollution. J Nat Hist 45:2397–2417

    Article  Google Scholar 

  • Nicol EAT (1935) The ecology of a salt-marsh. J Mar Biol Assoc UK 20:203–261

    Article  CAS  Google Scholar 

  • Núñez J, Brito MC, Docoito JR (2005) Anélidos poliquetos de Canarias: Catálogo de especies, distribución y hábitats. Vieraea 33:297–321

    Google Scholar 

  • Núñez J, Riera R, Brito MC (2010) Nuevos registros de poliquetos macrofaunales en las islas Salvajes. Vieraea 38:55–62

    Google Scholar 

  • Nygren A (2014) Cryptic polychaete diversity: a review. Zool Scripta 43:172–183

    Article  Google Scholar 

  • Nygren A, Pleijel F (2011) From one to ten in a single stroke—resolving the European Eumida sanguinea (Phyllodocidae, Annelida) species complex. Mol Phylogenet Evol 58:132–141

    Article  PubMed  Google Scholar 

  • Occhipinti Ambrogi A, Savini D (2003) Biological invasions as a component of global change in stressed marine ecosystems. Mar Pollut Bull 46:542–551

    Article  CAS  PubMed  Google Scholar 

  • Ojaveer H, Galil BS, Minchin D, Olenin S, Amorim A, Canning-Clode J, Chainho P, Copp GH, Gollasch S, Jelmertj A, Lehtiniemi M, McKenzie C, Mikuš J, Miossec L, Occhipinti-Ambrogi A, Pećarević M, Pederson J, Quilez-Badia G, Wijsman JWM, Zenetos A (2013) Ten recommendations for advancing the assessment and management of non-indigenous species in marine ecosystems. Mar Policy 44:160–165

    Article  Google Scholar 

  • Orensanz JM, Schwindt E, Pastorino G, Bortolus A, Casas G, Darrigran G, Elías R, López Gappa JJ, Obenat S, Pascual M, Penchaszadeh P, Piriz ML, Scarabino F, Spivak D, Vallarino EA (2002) No longer the pristine confines of the world ocean: a survey of exotic marine species in the southwestern Atlantic. Biol Invasions 4:115–143

    Article  Google Scholar 

  • Pimentel D, McNair S, Janecka J, Wightman J, Simmonds C, O’Connell C, Wong E, Russel L, Zern J, Aquino T, Tsomondo T (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84:1–20

    Article  Google Scholar 

  • Pollard DA, Hutchings PA (1990a) A review of exotic marine organisms introduced to the Australian region. I. Fishes. Asian Fish Sci 3:205–221

    Google Scholar 

  • Pollard DA, Hutchings PA (1990b) A review of exotic marine organisms introduced to the Australian region. II. Invertebrates. Asian Fish Sci 3:223–250

    Google Scholar 

  • Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol Ecol 21:1864–1877

    Article  CAS  PubMed  Google Scholar 

  • Rilov G, Crooks JA (2009) Biological invasions in marine ecosystems. Ecological, management, and geographical perspectives. Springer Verlag, Berlin

    Book  Google Scholar 

  • Rodrigo AP, Costa MH, Alves de Matos AP, Carrapiço F, Costa PM (2015) A study on the digestive physiology of a marine polychaete (Eulalia viridis) through microanatomical changes of epithelia during the digestive cycle. Microsc Microanal 21:91–101

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schimmenti E, Musco L, Lo Brutto S, Mikac B, Nygren A, Badalamenti F (2016) Mediterranean record of Eulalia ornata (Annelida: Phyllodocidae) corroborating its fidelity link with the Sabellaria alveolata reef habitat. Mediterr Mar Sci 17:359–370

    Article  Google Scholar 

  • Schwindt E, López Gappa J, Raffo MP, Tatián M, Bortolus A, Orensanz JM, Alonso G, Diez ME, Doti B, Genzano G, Lagger C, Lovrich G, Piriz ML, Méndez MM, Savoya V, Sueiro MC (2014) Marine fouling invasions in ports of Patagonia (Argentina) with implications for legislation and monitoring programs. Mar Environ Res 99:60–68

    Article  CAS  PubMed  Google Scholar 

  • Simboura N, Zenetos A (2005) Increasing polychaete diversity as a consequence of increasing research effort in Greek waters: new records and exotic species. Mediterr Mar Sci 6:75–88

    Article  Google Scholar 

  • Sun Y, Wong E, Keppel E, Williamson JE, Kupriyanova EK (2017) A global invader or a complex of regionally distributed species? Clarifying the status of an invasive calcareous tubeworm Hydroides dianthus (Verrill, 1873) (Polychaeta: Serpulidae) using DNA barcoding. Mar Biol 164:28

    Article  CAS  Google Scholar 

  • Tovar-Hernández MA, Yáñez-Rivera B, Bortolini-Rosales JL (2011) Reproduction of the invasive fan worm Branchiomma bairdi (Polychaeta: Sabellidae). Mar Biol Res 7:710–718

    Article  Google Scholar 

  • Vilà M, Basnou C, Pyšek P, Joseffson M, Genovesi P, Gollasch S, Nentwig W, Olenin S, Roques A, RoyD HPE, DAISIE partners (2010) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Fr Ecol Environ 8:135–144

    Article  Google Scholar 

  • Wittenberg R, Cock MJW (2001) Invasive alien species: a toolkit of best prevention and management practices. CAB International, Wallingford 228 pp

    Book  Google Scholar 

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Acknowledgements

We would like to thank Fabio Bulleri, Marco Casu and Chiara Ravaglioli for their help in sampling the Mediterranean specimens of Eulalia cf. clavigera; Michele Barbieri and Federica Squarcia for their support in the molecular laboratory work. Ana Parma and the late Lobo Orensanz enthusiastically shared their home and experience, and the latter also participated in the collecting trips in Puerto Madryn. Lastly, we are grateful to two anonymous reviewers that greatly contributed to the improvement of the manuscript.

Funding

The EC-funded project no. 295,213, RECOMPRA, FP7-PEOPLE-2011-IRSES funded the sampling of E. clavigera in Puerto Madryn by TVF and FB.

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Authors and Affiliations

  1. Department of Biology, University of Pisa, via Derna 1, 56126, Pisa, Italy

    Joachim Langeneck & Alberto Castelli

  2. Laboratorio de Parasitología (LAPA), Instituto de Biología de Organismos Marinos (IBIOMAR), (CCT-CONICET-CENPAT), Blvd. Brown, 2915, Puerto Madryn, Argentina

    María Emilia Diez

  3. Sjöfartsmuseet Akvariet, Karl Johansgatan 1-3, 41459, Göteborg, Sweden

    Arne Nygren

  4. Depto. Sistemática y Ecología Acuática, El Colegio de la Frontera Sur, Chetumal, Quintana Roo, Mexico

    Sergio Salazar-Vallejo & Luis Fernando Carrera-Parra

  5. National Research Council (CNR)—Institute of Coastal Marine Environment (IAMC), Calata Porta di Massa, 80133, Naples, Italy

    Tomás Vega Fernández

  6. Stazione Zoologica Anton Dohrn, Villa Comunale, 80121, Naples, Italy

    Tomás Vega Fernández, Fabio Badalamenti & Luigi Musco

  7. National Research Council (CNR)—Institute of Coastal Marine Environment (IAMC), Marine Ecology Laboratory, Via Giovanni da Verrazzano 17, 91014, Castellammare del Golfo, Italy

    Fabio Badalamenti

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  1. Joachim Langeneck
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  2. María Emilia Diez
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  4. Sergio Salazar-Vallejo
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Correspondence to Joachim Langeneck.

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Langeneck, J., Diez, M.E., Nygren, A. et al. Worming its way into Patagonia: an integrative approach reveals the cryptic invasion by Eulalia clavigera (Annelida: Phyllodocidae). Mar Biodiv 49, 851–861 (2019). https://doi.org/10.1007/s12526-018-0864-y

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