Biological Invasions

, Volume 18, Issue 4, pp 1203–1215 | Cite as

When invasion biology meets taxonomy: Clavelina oblonga (Ascidiacea) is an old invader in the Mediterranean Sea

  • Víctor Ordóñez
  • Marta Pascual
  • Margarita Fernández-Tejedor
  • Xavier Turon
Original Paper


Taxonomic issues often confound the study of invasive species, which sometimes are unrecognized as introduced in newly colonized areas. Clavelina oblonga Herdman, 1880 is an abundant ascidian species along the southeastern coast of the United States and the Caribbean Sea. It was introduced into the eastern Atlantic and Brazil decades ago. In the Mediterranean Sea, a similar species had been described as C. phlegraea Salfi 1929 and reported from southern Italy and Corsica. In the last few years a species of Clavelina has proliferated in the embayments of the Ebro Delta (NW Mediterranean), a zone of active bivalve culture industry where it has smothered mussel spat, leading to economic loss. We here report the morphological and genetic identity of this species, synonymizing the Atlantic C. oblonga and the Mediterranean C. phlegraea (the latter therefore is a synonym of the former). Thus, C. oblonga has existed in the Mediterranean for over 80 years, but was known under a different name. We also found this species in natural habitats in the Iberian Atlantic coast close to the Strait of Gibraltar, raising concerns about an ongoing expansion. In order to obtain information relevant for management, we monitored growth, reproductive cycles and settlement patterns of this ascidian on bivalve cultures in the Ebro Delta. Its biological cycles were markedly seasonal, with peak abundance and reproduction during the warmest months, followed by regression during the cold season. The settlement period was short, mostly concentrated in a single month each year. Avoidance of mussel and oyster seeding during late summer and early autumn can readily reduce the damage caused by this species.


Ascidian Clavelina phlegraea Life cycle Recruitment Aquaculture pest Fouling 



We thank all who contributed samples and field assistance, including F. Monniot for specimens from Urbino Lagoon, F. Boero and G. Farella from Mar Piccolo of Taranto, P. Wirtz from Azores. P. Sordino, G. Procaccini, and S. d’Aniello helped in the type locality of Naples. We thank R. Arizmendi, G. Calabria, M. Clusa, R. Márquez, M.C. Pineda and C. Pegueroles for monitoring help, and M. Fernández and C. Miralpeix for laboratory assistance. We thank M. Cuñarro for the treatment of the images, J.M. Reverte for field work and A. Bertomeu for the rope deployment in his premises. We also thank C.A. Stepien for insightful manuscript edits. V.O. was supported by a FPU PhD scholarship (AP2008/04209) from the Spanish Ministerio de Educación. The authors are part of the research group SGR2014-336 of the Generalitat de Catalunya (Spain). This research was funded by the COCONET project #287844 of the 7th European Community Framework Program and by Spanish Government projects CTM2010-22218 and CTM2013-48163.

Supplementary material

10530_2016_1062_MOESM1_ESM.docx (892 kb)
Supplementary material 1 (DOCX 892 kb)


  1. Brunetti R (1987) Species of Clavelina in the Mediterranean Sea. Ann Inst Oceanogr Paris 63:553–930Google Scholar
  2. Bullard SG, Lambert G, Carman MR, Byrnes J, Whitlatch RB, Ruiz G, Miller RJ, Harris L, Valentine PC, Collie JS, Pederson J, McNaught DC, Cohen AN, Asch RG, Dijkstra J, Heinonen K (2007) The colonial ascidian Didemnum sp. A: current distribution, basic biology, and potential threat to marine communities of the northeast and west coasts of North America. J Exp Mar Biol Ecol 342:99–108CrossRefGoogle Scholar
  3. Camp J, Delgado M (1987) Hidrografía de las bahías del Delta del Ebro. Inv Pesq 51:351–369Google Scholar
  4. Carlton JT (2009) Deep invasion ecology and the assembly of communities in historical time. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems: ecological, management, and geographic perspectives. Springer, Berlin, pp 13–56CrossRefGoogle Scholar
  5. Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82CrossRefGoogle Scholar
  6. Castilla JC, Lagos NA, Cerda M (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Mar Ecol Prog Ser 268:119–130CrossRefGoogle Scholar
  7. Cordell JR, Levy C, Toft JD (2013) Ecological implications of invasive tunicates associated with artificial structures in Puget Sound, Washington, USA. Biol Invasions 15:1303–1318CrossRefGoogle Scholar
  8. Daigle RM, Herbinger CM (2009) Ecological interactions between the vase tunicate (Ciona intestinalis) and the farmed mussel (Mytilus edulis) in Nova Scotia, Canada. Aquat Invasions 4:177–187CrossRefGoogle Scholar
  9. De Caralt S, López-Legentil S, Tarjuelo I, Uriz MJ, Turon X (2002) Contrasting biological traits of Clavelina lepadiformis (Ascidiacea) populations from inside and outside harbours in the western Mediterranean. Mar Ecol Prog Ser 244:125–137CrossRefGoogle Scholar
  10. De Pippo T, Donadio C, Grottola D, Pennetta M (2004) Geomorphological evolution and environmental reclamation of Fusaro Lagoon (Campania Province, southern Italy). Environ Int 30:199–208CrossRefPubMedGoogle Scholar
  11. Fitridge I, Dempster T, Guenther J, De Nys R (2012) The impact and control of biofouling in marine aquaculture: a review. Biofouling 28:649–669CrossRefPubMedGoogle Scholar
  12. Fletcher LM, Forrest BM, Bell JJ (2013) Impacts of the invasive ascidian Didemnum vexillum on green-lipped mussel Perna canaliculus aquaculture in New Zealand. Aquac Environ Inter 4:17–30CrossRefGoogle Scholar
  13. 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 Biotech 3:294–299Google Scholar
  14. Goldstien SJ, Dupont L, Viard F, Hallas PJ, Nishikawa T, Schiel DR, Gemmell NJ, Bishop JDD (2011) Global phylogeography of the widely introduced North West Pacific ascidian Styela clava. PLoS ONE 6:e16755CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gollasch S (2006) Overview on introduced aquatic species in European navigational and adjacent waters. Helgol Mar Res 60:84–89CrossRefGoogle Scholar
  16. Hartmeyer R (1912) Die ascidien der Deutschen Tiefsee-Expedition. Deutschen Tiefsee-Expedit 16:225–392Google Scholar
  17. Kott P (1985) The Australian Ascidiacea. Part I. Phlebobranchia and Stolidobrancyhia. Mem Qld Mus 23:1–440Google Scholar
  18. Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4CrossRefGoogle Scholar
  19. Lambert G (2009) Adventures of a sea squirt sleuth: unraveling the identity of Didemnum vexillum, a global ascidian invader. Aquat Invasions 4:5–28CrossRefGoogle Scholar
  20. Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161CrossRefGoogle Scholar
  21. López-Legentil S, Ruchty M, Domenech A, Turon X (2005) Life cycles and growth rates of two morphotypes of Cystodytes (Ascidiacea) in the western Mediterranean. Mar Ecol Prog Ser 296:219–228CrossRefGoogle Scholar
  22. López-Legentil S, Legentil ML, Erwin PM, Turon X (2015) Harbor networks as introduction gateways: contrasting distribution patterns of native and introduced species. Biol Invasions 17:1623–1638CrossRefPubMedPubMedCentralGoogle Scholar
  23. Madariaga DJ, Rivadeneira MM, Tala F, Thiel M (2014) Environmental tolerance of the two invasive species Ciona intestinalis and Codium fragile: their invasive potential along a temperate coast. Biol Invasions 16:2507–2527CrossRefGoogle Scholar
  24. Mastrototaro F, D’Onghia G, Tursi A (2008) Spatial and seasonal distribution of ascidians in a semi-enclosed basin of the Mediterranean Sea. J Mar Biol Ass UK 88:1053–1061Google Scholar
  25. McGlashan DJ, Ponniah M, Cassey P, Viard F (2008) Clarifying marine invasions with molecular markers: an illustration based on mtDNA from mistaken calyptraeid gastropod identifications. Biol Invasions 10:51–57CrossRefGoogle Scholar
  26. Minchin D (2007) Aquaculture and transport in a changing environment: overlap and links in the spread of alien biota. Mar Pollut Bull 55:302–313CrossRefPubMedGoogle Scholar
  27. Monniot F (1974) Ascidies littorales et bathyales récoltées au cours de la campagne Biaçores: aplousobranches. Bull Mus Natl Hist Nat 251:1287–1325 3e ser Google Scholar
  28. Monniot F, Giannesini PJ, Oudot J, Richard ML (1986) Ascidies: “salissures” marines et indicateurs biologiques (métaux, hydrocarbures). Bull Mus Natl Hist Nat 8:215–245 4e Ser Google Scholar
  29. Naylor RL, Williams SL, Strong DR (2001) Aquaculture—a gateway for exotic species. Science 294:1655–1656CrossRefPubMedGoogle Scholar
  30. Ordóñez V, Rius M, McQuaid CD, Pineda MC, Pascual M, Turon X (2013) Early biotic interactions among introduced and native benthic species reveal cryptic predation and shifts in larval behavior. Mar Ecol Prog Ser 488:65–79CrossRefGoogle Scholar
  31. Ordóñez V, Pascual M, Fernández-Tejedor M, Pineda MC, Tagliapietra D, Turon X (2015) Ongoing expansion of the worldwide invader Didemnum vexillum (Ascidiacea) in the Mediterranean Sea: high plasticity of its biological cycle promotes establishment in warm waters. Biol Invasions 17:2075–2085CrossRefPubMedPubMedCentralGoogle Scholar
  32. Pérès JM (1951) Nouvelle contribution à l’étude des ascidies de la Cote occidentale d’Afrique. Bull Inst Fondam Afr Noire A13:1051–1071Google Scholar
  33. Pineda MC, McQuaid CD, Turon X, López-Legentil S, Ordóñez V, Rius M (2012) Tough adults, frail babies: an analysis of stress sensitivity across early life-history stages of widely introduced marine invertebrates. PLoS ONE 7(19):e46672CrossRefPubMedPubMedCentralGoogle Scholar
  34. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  35. Ramsay A, Davidson J, Bourque D, Stryhn H (2009) Recruitment patterns and population development of the invasive ascidian Ciona intestinalis in Prince Edwards Island, Canada. Aquat Invasions 4:169–176CrossRefGoogle Scholar
  36. Rocha RM (1991) Replacement of the compound ascidian species in a southeastern Brazilian fouling community. Bol Inst Oceanogr Sao Paulo 39:141–153Google Scholar
  37. Rocha RM, Kremer LP, Fehlauer-Ale KH (2012) Lack of COI variation for Clavelina oblonga (Tunicata, Ascidiacea) in Brazil: evidence for its human-mediated transportation? Aquat Invasions 7:419–424CrossRefGoogle Scholar
  38. Salfi M (1929) Sulla blastogenesi in Clavelina e su una nuova specie del genere. Pub Staz Zool Napoli 9:195–201Google Scholar
  39. Stefaniak L, Zhang H, Gittenberger A, Smith K, Holsinger Lin S, Whitlatch RB (2012) Determining the native region of the putatively invasive ascidian Didemnum vexillum Kott, 2002. J Exp Mar Biol Ecol 422–423:64–71CrossRefGoogle Scholar
  40. Turon X, Tarjuelo I, Duran S, Pascual M (2003) Characterizing invasion processes with genetic data: an Atlantic clade of Clavelina lepadiformis (Ascidiacea) introduced into Mediterranean harbours. Hydrobiologia 503:29–35CrossRefGoogle Scholar
  41. Van Name WG (1945) The North and South American ascidians. Bull Am Mus Nat Hist 84:1–476Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Víctor Ordóñez
    • 1
  • Marta Pascual
    • 1
  • Margarita Fernández-Tejedor
    • 2
  • Xavier Turon
    • 3
  1. 1.Department of Genetics and IRBioUniversity of BarcelonaBarcelonaSpain
  2. 2.Institute of Agriculture and Food Research and Technology (IRTA)S. Carles de la RàpitaSpain
  3. 3.Center for Advanced Studies of Blanes (CEAB-CSIC)Blanes, GironaSpain

Personalised recommendations