Marine Biodiversity

, Volume 49, Issue 2, pp 851–861 | Cite as

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

  • Joachim LangeneckEmail author
  • María Emilia Diez
  • Arne Nygren
  • Sergio Salazar-Vallejo
  • Luis Fernando Carrera-Parra
  • Tomás Vega Fernández
  • Fabio Badalamenti
  • Alberto Castelli
  • Luigi Musco
Original Paper


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.


Non-native species Phyllodocidae Predation Cryptogenic species Species complex Molecular characterisation 



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.


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.

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Field study

Permits and approval of field or observational studies have been obtained by the authors.


  1. 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 105–209Google Scholar
  2. 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 plsGoogle Scholar
  3. 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 157:69–80CrossRefGoogle Scholar
  4. 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 130:325–337CrossRefGoogle Scholar
  5. 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 17:3684–3696CrossRefGoogle Scholar
  6. 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 62:129–141Google Scholar
  7. 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 33:263–271CrossRefGoogle Scholar
  8. 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 37:33–48Google Scholar
  9. 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 66:84–96CrossRefGoogle Scholar
  10. 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 3:265–273CrossRefGoogle Scholar
  11. Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77:1653–1655CrossRefGoogle Scholar
  12. 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:e22232Google Scholar
  13. 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 2880:51–64CrossRefGoogle Scholar
  14. Çinar ME (2013) Alien polychaete species worldwide: current status and their impacts. J Mar Biol Assoc UK 93:1257–1278CrossRefGoogle Scholar
  15. 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 31:403–410Google Scholar
  16. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166CrossRefGoogle Scholar
  17. 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 83:233–243CrossRefGoogle Scholar
  18. 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 ppGoogle Scholar
  19. Emson RH (1977) The feeding and consequent role of Eulalia viridis (O.F. Müller) (Polychaeta) in intertidal communities. J Mar Biol Assoc UK 57:93–96CrossRefGoogle Scholar
  20. Evans RG (1949) The intertidal ecology of rocky shores in south Pembrokeshire. J Ecol 37:120–139CrossRefGoogle Scholar
  21. 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 1847:1–18Google Scholar
  22. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 4:783–791CrossRefGoogle Scholar
  23. 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 3:294–299Google Scholar
  24. Giangrande A (2003) Biodiversity, conservation and the ‘taxonomic impediment’. Aquat Conserv 13:451–459CrossRefGoogle Scholar
  25. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp Ser 41:95–98Google Scholar
  26. Holloway MG, Keough MJ (2002) Effects of an introduced polychaete, Sabella spallanzanii, on the development of epifaunal assemblages. Mar Ecol Prog Ser 236:137–154CrossRefGoogle Scholar
  27. Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18CrossRefGoogle Scholar
  28. 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 28:1188–1194CrossRefGoogle Scholar
  29. Kato T, Pleijel F, Mawatari SF (2001) Eulalia gemina (Phyllodocidae: Polychaeta), a new species form Shirahama. Jpn Proc Biol Soc Wash 114:381–388Google Scholar
  30. Kensler CB (1967) Desiccation resistance of intertidal crevice species as a factor in their zonation. J Anim Ecol 36:391–406CrossRefGoogle Scholar
  31. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefGoogle Scholar
  32. Kinberg JGH (1866) Annulata nova (Nephthydea, Phyllodocea, Alciopea, Hesionida, Glycerea, Goniadea, Syllidea, Ariciea, Spiodea, Aonidea, Cirratulida, Opheliacea). Kongelige Vetenskaps-Akademiens Förhandlingar 22:239–258Google Scholar
  33. 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 2:33–78Google Scholar
  34. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  35. 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 23:947–2948CrossRefGoogle Scholar
  36. Leppäkoski E, Gollasch S, Olenin S (2002) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer Academic Publishers, Dordrecht, p 583CrossRefGoogle Scholar
  37. 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 16:298–313CrossRefGoogle Scholar
  38. 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 16:2035–2054CrossRefGoogle Scholar
  39. Marchini A, Galil BS, Occhipinti-Ambrogi A (2015) Recommendations on standardizing lists of marine alien species: lessons from the Mediterranean Sea. Mar Pollut Bull 101:267–273CrossRefGoogle Scholar
  40. Michel C (1970) Role physiologique de la trompe chez quatre annelides polychètes appartenant aux genres: Eulalia, Phyllodoce, Glycera et Notomastus. Cah Biol Mar 11:209–228Google Scholar
  41. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Fr Ecol Environ 6:485–492CrossRefGoogle Scholar
  42. Morgado EH, Amaral ACZ (1984) Anelídeos poliquetos asociados ao briozário Schizoporella unicornis (Johnston), 4. Phyllodocidae e Hesionidae. Rev Bras Zool 2:49–54CrossRefGoogle Scholar
  43. 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 45:2397–2417CrossRefGoogle Scholar
  44. Nicol EAT (1935) The ecology of a salt-marsh. J Mar Biol Assoc UK 20:203–261CrossRefGoogle Scholar
  45. Núñez J, Brito MC, Docoito JR (2005) Anélidos poliquetos de Canarias: Catálogo de especies, distribución y hábitats. Vieraea 33:297–321Google Scholar
  46. Núñez J, Riera R, Brito MC (2010) Nuevos registros de poliquetos macrofaunales en las islas Salvajes. Vieraea 38:55–62Google Scholar
  47. Nygren A (2014) Cryptic polychaete diversity: a review. Zool Scripta 43:172–183CrossRefGoogle Scholar
  48. 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 58:132–141CrossRefGoogle Scholar
  49. Occhipinti Ambrogi A, Savini D (2003) Biological invasions as a component of global change in stressed marine ecosystems. Mar Pollut Bull 46:542–551CrossRefGoogle Scholar
  50. 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 44:160–165CrossRefGoogle Scholar
  51. 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 4:115–143CrossRefGoogle Scholar
  52. 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 84:1–20CrossRefGoogle Scholar
  53. Pollard DA, Hutchings PA (1990a) A review of exotic marine organisms introduced to the Australian region. I. Fishes. Asian Fish Sci 3:205–221Google Scholar
  54. Pollard DA, Hutchings PA (1990b) A review of exotic marine organisms introduced to the Australian region. II. Invertebrates. Asian Fish Sci 3:223–250Google Scholar
  55. Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol Ecol 21:1864–1877CrossRefGoogle Scholar
  56. Rilov G, Crooks JA (2009) Biological invasions in marine ecosystems. Ecological, management, and geographical perspectives. Springer Verlag, BerlinCrossRefGoogle Scholar
  57. 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 21:91–101CrossRefGoogle Scholar
  58. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  59. 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 17:359–370CrossRefGoogle Scholar
  60. 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 99:60–68CrossRefGoogle Scholar
  61. 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 6:75–88CrossRefGoogle Scholar
  62. 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 164:28CrossRefGoogle Scholar
  63. Tovar-Hernández MA, Yáñez-Rivera B, Bortolini-Rosales JL (2011) Reproduction of the invasive fan worm Branchiomma bairdi (Polychaeta: Sabellidae). Mar Biol Res 7:710–718CrossRefGoogle Scholar
  64. 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 8:135–144CrossRefGoogle Scholar
  65. Wittenberg R, Cock MJW (2001) Invasive alien species: a toolkit of best prevention and management practices. CAB International, Wallingford 228 ppCrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Joachim Langeneck
    • 1
    Email author
  • María Emilia Diez
    • 2
  • Arne Nygren
    • 3
  • Sergio Salazar-Vallejo
    • 4
  • Luis Fernando Carrera-Parra
    • 4
  • Tomás Vega Fernández
    • 5
    • 6
  • Fabio Badalamenti
    • 6
    • 7
  • Alberto Castelli
    • 1
  • Luigi Musco
    • 6
  1. 1.Department of BiologyUniversity of PisaPisaItaly
  2. 2.Laboratorio de Parasitología (LAPA), Instituto de Biología de Organismos Marinos (IBIOMAR), (CCT-CONICET-CENPAT)Puerto MadrynArgentina
  3. 3.Sjöfartsmuseet AkvarietGöteborgSweden
  4. 4.Depto. Sistemática y Ecología AcuáticaEl Colegio de la Frontera SurChetumalMexico
  5. 5.National Research Council (CNR)—Institute of Coastal Marine Environment (IAMC)NaplesItaly
  6. 6.Stazione Zoologica Anton DohrnNaplesItaly
  7. 7.National Research Council (CNR)—Institute of Coastal Marine Environment (IAMC), Marine Ecology LaboratoryCastellammare del GolfoItaly

Personalised recommendations