Skip to main content
SpringerLink
Log in

Pathways of spread of the introduced ascidian Styela clava (Tunicata) in Northern Europe, as revealed by microsatellite markers

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Styela clava, a solitary ascidian native to the NW Pacific, has become a conspicuous member of fouling communities in NW European waters. As its natural dispersal appears to be limited, the wide distribution of S. clava along coasts within its introduced range may be attributed to secondary spread assisted by human activities. Here, we used six microsatellite loci to examine the genetic diversity and extent of gene flow among S. clava populations in its European introduced range. Samples were collected from 21 populations within Europe (N = 808), 4 populations within the USA and two populations within the native range (Japan). Large variation in genetic diversity was observed among the European populations but were not explained either by the geographic distance from the first introduction area (i.e. Plymouth, UK) nor by the time elapsed since the introduction. No founder effect was observed in the introduced populations, except possibly in Puget Sound (USA). At least two different introductions occurred in Europe, identified as distinct genetic clusters: northern Danish populations (resembling one Japanese population), and the rest of Europe; a sample from Shoreham (England) possibly represents a third introduction. In North America, the population from the Atlantic was genetically similar to the majority of European populations, suggesting a European origin for populations on this seaboard, while populations from the Pacific coast were genetically similar to the same Japanese population as the Danish populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abbott PD, Johnson JV (1972) The ascidians Styela barnharti, S. plicata, S. clava and S. montereyensis in Californian waters. Bull South Calif Acad Sci 71:95–105

    Google Scholar 

  • Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows pour la génétique des populations. Laboratoire Génome, Population, Interactions, CNRS UMR 5000, Université Montpellier II, Montpellier

  • Ben-Schlomo R, Paz G, Rinkevich B (2006) Postglacial-period and recent invasions shape the population genetics of botryllid ascidians along European Atlantic coasts. Ecosystems 9:1118–1127

    Article  Google Scholar 

  • Ben-Shlomo R, Douek J, Rinkevich B (2001) Heterozygote deficiency and chimerism in remote populations of a colonial ascidian from New Zealand. Mar Ecol Prog Ser 209:109–117

    Article  Google Scholar 

  • Berman J, Harris L, Lambert W, Buttrick M, Dufresne M (1992) Recent invasions of the Gulf of Maine—3 contrasting ecological histories. Conserv Biol 6:435–441

    Article  Google Scholar 

  • Bishop MWH (1947) Establishment of an immigrant barnacle in British coastal waters. Nature 159:501–502

    Article  Google Scholar 

  • Bourque D, Davidson J, MacNair NG, Arsenault G, LeBlanc AR, Landry T, Miron G (2007) Reproduction and early life history of an invasive ascidian Styela clava Herdman in Prince Edward Island, Canada. J Exp Mar Biol Ecol 342:78–84

    Article  Google Scholar 

  • Breton G, Dupont W (1973) Styela clava Herdmann, ascidie nouvelle pour les côtes de la baie de Seine abonde dans le port du Havre (76). Bull Trimest Soc Géol Normandie 65:32

    Google Scholar 

  • Brunetti R (1979) Polyandrocarpa zorritensis (Van Name, 1931) a colonial ascidian new to Mediterranean record. Vie Milieu 29:647–652

    Google Scholar 

  • Buizer DAG (1980) Explosive development of Styela clava Herdman 1882, in the Netherlands after its introduction (Tunicata ascidiacea). Bull Zool Mus Univ Amsterdam 7:181–187

    Google Scholar 

  • Carlisle DB (1954) Styela mammiculata N.SP., a new species of ascidian from the Plymouth area. J Mar Biol Ass UK 33:329–334

    Article  Google Scholar 

  • Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biol Conserv 78:97–106

    Article  Google Scholar 

  • Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Article  Google Scholar 

  • Castilla JC, Collins AG, Meyer CP, Guinez R, Lindberg DR (2002) Recent introduction of the dominant tunicate, Pyura praeputialis (Urochordata, Pyuridae) to Antofagasta, Chile. Mol Ecol 11:1579–1584

    Article  CAS  PubMed  Google Scholar 

  • Castilla JC, Guinez R, Caro AU, Ortiz V (2004) Invasion of a rocky intertidal shore by the tunicate Pyura praeputialis in the Bay of Antofagasta, Chile. Proc Natl Acad Sci USA 101:8517–8524

    Article  CAS  PubMed  Google Scholar 

  • Christiansen J, Thomsen JC (1981) Styela clava Herdman 1882, a species new to the Danish fauna (Tunicata, Ascidiacea). Steenstrupia 7:15–24

    Google Scholar 

  • Cohen AN, Carlton JT (1995) Nonindigenous aquatic in a United States estuary: a case of the biological invasions of the San Francisco Bay and Delta. A report for the United States Fish and Wildlife service, Washington DC and the National Sea Grant College Program, Connecticut State Grant (NOAA Grant Number NA36RG0467)

  • Cohen AN, Mills C, Berry H, Wonham M, Bingham B, Bookheim B, Carlton JT, Chapman J, Cordell J, Harris L, Klinger T, Kohn A, Lambert CC, Lambert G, Li K, Secord D, Toft J (1998) Report of the Puget Sound Expedition September 8–16, 1998. A rapid assessment survey of non-indigenous species in the shallow waters of Puget Sound, Washington State Department of Natural Resources, Olympia, WA. United States Fish and Wildlife Service, Lacey

  • Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843

    Article  PubMed  Google Scholar 

  • Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374

    CAS  PubMed  Google Scholar 

  • Corander J, Siren J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129

    Article  Google Scholar 

  • Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  Google Scholar 

  • Coughlan J (1969) The leathery sea-squirt—a new ascidian from Milford Haven. Nat Wales 11:192–193

    Google Scholar 

  • Coughlan J (1985) Occurrence of the immigrant ascidian Styela clava Herdman in Heysham harbour, Lancashire. Porc Mar Nat Hist Soc Newsl 3:85–87

    Google Scholar 

  • Davis MH, Davis ME (2004a) The distribution limits of Styela clava (Tunicata, Ascidiacea) in European waters. Porc Mar Nat Hist Soc Newsl 15:35–43

    Google Scholar 

  • Davis MH, Davis ME (2004b) New records of Styela clava Herdman, 1882 (Tunicata, Ascidiacea) in Europe. Porc Mar Nat Hist Soc Newsl 14:24–28

    Google Scholar 

  • Davis MH, Davis ME (2006) Styela clava (Tunicata, Ascidiacea)—a new addition to the fauna of New Zealand. Porc Mar Nat Hist Soc Newsl 20:19–22

    Google Scholar 

  • Davis MH, Davis ME (2008) First record of Styela clava (Tunicata, Ascidiacea) in the Mediterranean region. Aquat Invasions 3:125–132

    Article  Google Scholar 

  • Di Rienzo A, Peterson AC, Garcza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  CAS  PubMed  Google Scholar 

  • Dupont L, Viard F, Bishop JDD (2006) Isolation and characterization of twelve polymorphic microsatellite markers for the invasive ascidian Styela clava (Tunicata). Mol Ecol Notes 6:101–103

    Article  CAS  Google Scholar 

  • Dupont L, Viard F, David P, Bishop JDD (2007) Combined effects of bottlenecks and selfing in populations of Corella eumyota, a recently introduced sea squirt in the English Channel. Diversity Distrib 13:808–817

    Article  Google Scholar 

  • Dupont L, Viard F, Dowell MJ, Wood C, Bishop JDD (2009) Fine- and regional-scale genetic structure of the exotic ascidian Styela clava (Tunicata) in south-west England, 50 years after its introduction. Mol Ecol 18:442–453

    Article  CAS  PubMed  Google Scholar 

  • Eckert CG, Manicacci D, Barrett SCH (1996) Genetic drift and founder effect in native versus introduced populations of an invading plant, Lythrum salicaria (Lythraceae). Evolution 50:1512–1519

    Article  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree Argania spinosa (L.) Skeels endemic to Morocco. Theorl Appl Genet 92:832–839

    Article  Google Scholar 

  • Goudet J (1999) FSTAT vers. 2.8, updated from Goudet (1995). Fstat: a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Goulletquer P, Bachelet G, Sauriau PG, Noel P (2002) Open Atlantic coast of Europe—a century of introduced species into French waters. In: Leppäkoski E, Gollash S, Olenin S (eds) Invasive aquatic species of Europe. Kluwer, Dordrecht

    Google Scholar 

  • Guiry GM, Guiry MD (1973) Spread of an introduced ascidian to Ireland. Mar Poll Bull 4:127

    Article  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Associates, Sunderland

    Google Scholar 

  • Herdman WA (1882) Report on the Tunicata collected during the voyage of H.M.S. Challenger during the years 1873–76. Part I.-Ascidiæ simplices. Zool Chall Exped 6:1–296

    Google Scholar 

  • Holmes NJ (1968) Aspects of the biology of Styela clava Herdman. PhD thesis, University of Southampton

  • Huwae PHM, Lavaleye MSS (1975) Styela clava Herdman, 1882 (Tunicata, Ascidiacea) nieuw voor Nederland. Zool Bijdr 17:79–81

    Google Scholar 

  • Knudsen J (1989) Immigration of marine invertebrates to the Limfjord (Denmark) and the North Sea—Baltic transition area. In: Steinberger Y, Luria M, Spanier E (eds) Environmental quality and ecosystem stability. ISEEQ, Jerusalem, pp 135–145

    Google Scholar 

  • Lambert G (2004) The south temperate and Antarctic ascidian Corella eumyota reported in two harbours in north-western France. J Mar Biol Assoc UK 84:239–241

    Article  Google Scholar 

  • Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4

    Article  Google Scholar 

  • Lambert CC, Lambert G (1998) Non-indigenous ascidians in southern California harbors and marinas. Mar Biol 130:675–688

    Article  Google Scholar 

  • Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161

    Article  Google Scholar 

  • Locke A, Hanson JM, Ellis KM, Thompson J, Rochette R (2007) Invasion of the southern Gulf of St. Lawrence by the clubbed tunicate (Styela clava Herdman): potential mechanisms for invasions of Prince Edward Island estuaries. J Exp Mar Biol Ecol 342:69–77

    Article  Google Scholar 

  • Lopez-Legentil S, Turon X, Planes S (2006) Genetic structure of the star sea squirt, Botryllus schlosseri, introduced in southern European harbours. Mol Ecol 15:3957–3967

    Article  CAS  PubMed  Google Scholar 

  • Lützen J (1999) Styela clava Herdman (Urochordata, Ascidiacea), a successful immigrant to North West Europe: ecology, propagation and chronology of spread. Helgol Meeresunters 52:383–391

    Article  Google Scholar 

  • Lützen J, Sørensen V (1993) Ecology, reproduction and further spread of the immigrant East-Asiatic ascidian Styela clava Herdman in Danish waters. Flora Fauna 2:75–79

    Google Scholar 

  • Millar RH (1960) The identity of the ascidians Styela mammiculata Carlisle and S. clava, Herdman. J Mar Biol Assoc UK 39:509–511

    Article  Google Scholar 

  • Minchin D, Duggan CB (1988) The distribution of the exotic ascidian, Styela clava, Herdman, in Cork harbour. Irish Nat J 22:388–393

    Google Scholar 

  • Monniot C (1981) Apparition de l’ascidie Microcosmus exasperatus dans les ports méditerrannéens. Tethys 10:59–62

    Google Scholar 

  • Monro CCA (1938) On a new species of serpulid polychaete from the Shoreham Harbour Canal, Sussec. Ann Mag Nat Hist 1:73–78

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Osman RW, Whitlatch RB (1999) Ecological interactions of invading ascidians within epifaunal communities of southern New England. In: Pederson J (ed) Marine bioinvasions: proceedings of conference January 24–27, 1999. Massachusetts Institute of Technology, Cambridge, Massachusetts, pp 164–174

  • Paz G, Douek J, Mo CQ, Goren M, Rinkevich B (2003) Genetic structure of Botryllus schlosseri (Tunicata) populations from the Mediterranean coast of Israel. Mar Ecol Prog Ser 250:153–162

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rinkevich B, Paz G, Douek J, Ben-Schlomo R (2001) Allorecognition and microsatellite allele polymorphism of Botryllus schlosseri from the Adriatic Sea. In: Sawada H, Yokosawa H, Lambert CC (eds) The biology of Ascidians. Springer, Tokyo, pp 426–435

    Google Scholar 

  • Rius M, Pascual M, Turon X (2008) Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidiacea) reveals high genetic diversity of introduced populations and non-independent colonizations. Divers Distrib 14:818–828

    Article  Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  • Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632

    Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular clonning. A laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Silva N, Smith WC (2008) Inverse correlation of population similarity and introduction date for invasive ascidians. PLoS One 3:e2552

    Article  PubMed  CAS  Google Scholar 

  • Simon-Bouhet B, Garcia-Meunier P, Viard F (2006) Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France: evidence from mitochondrial sequence data. Mol Ecol 15:1699–1711

    Article  CAS  PubMed  Google Scholar 

  • Stoner DS, Ben-Schlomo R, Rinkevich B, Weissman IL (2002) Genetic variability of Botryllus schlosseri invasions to the east and west coasts of the USA. Mar Ecol Prog Ser 243:93–100

    Article  Google Scholar 

  • Valentine PC, Collie JS, Reid RN, Asch RG, Guida VG, Blackwood DS (2007) The occurrence of the colonial ascidian Didemnum sp on Georges Bank gravel habitat—ecological observations and potential effects on groundfish and scallop fisheries. J Exp Mar Biol Ecol 342:179–181

    Article  Google Scholar 

  • Vázquez E, Urgorri V (1992) Ascidians of the fouling in the Ría de Ferrol. Nova Acta Científ Compostel 3:161–167

    Google Scholar 

  • Vermeij GJ (1996) An agenda for invasion biology. Biol Conserv 78:3–9

    Article  Google Scholar 

  • Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversity across introduced regions in a brown alga: Aquaculture vs. maritime traffic effects. Proc Natl Acad Sci USA 102:5432–5437

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed  Google Scholar 

  • Zibrowius H (1991) Ongoing modification of the Mediterranean marine fauna and flora by the establishment of exotic species. Mésogée 51:83–107

    Google Scholar 

Download references

Acknowledgments

This research was supported by the European Network of Excellence “Marine Genomics Europe” (contract no. 505403) and the NERC (UK) Oceans 2025 programme. FV and JB are the beneficiaries of a financial contribution from the AXA Research Fund (AXA Marine Aliens and Climate Change Project). We thank G. & C. Lambert, J. Lützen, D. Minchin and X. Turon for collecting and sending specimens. The authors are also grateful to two anonymous referees for points that improved the manuscript.

Author information

Authors and Affiliations

  1. Marine Biological Association, Citadel Hill, Plymouth, PL1 2PB, UK

    L. Dupont & J. D. D. Bishop

  2. UPMC Univ Paris 06, UMR 7144, Equipe Div&Co, Station Biologique, 29682, Roscoff, France

    F. Viard

  3. CNRS, UMR 7144, Adaptation & Diversité en Milieu Marin, Station Biologique, 29682, Roscoff, France

    F. Viard

  4. Nuclear Department, HMS Sultan, Military Road, Gosport, Hampshire, PO12 3BY, UK

    M. H. Davis

  5. Nagoya University Museum, Chikusa-ku, Nagoya, 464-8601, Japan

    T. Nishikawa

  6. School of Biological Sciences, University of Plymouth, Plymouth, PL4 8AA, UK

    J. D. D. Bishop

  7. UMR 7618 BioEMCo, Equipe IBIOS, Université Paris-Est, 61 avenue du Général de Gaulle, 94010, Créteil Cedex, France

    L. Dupont

Authors
  1. L. Dupont
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Viard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. H. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Nishikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. D. D. Bishop
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Dupont.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dupont, L., Viard, F., Davis, M.H. et al. Pathways of spread of the introduced ascidian Styela clava (Tunicata) in Northern Europe, as revealed by microsatellite markers. Biol Invasions 12, 2707–2721 (2010). https://doi.org/10.1007/s10530-009-9676-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-009-9676-0

Keywords

Search

Navigation