Marine Biology

, 162:0 | Cite as

Ascidians as models for studying invasion success

  • Aibin Zhan
  • Elizabeta Briski
  • Dan G. Bock
  • Sara Ghabooli
  • Hugh J. MacIsaac
Invasive Species - Review
Part of the following topical collections:
  1. Invasive Species


During the past three decades, coastal marine waters have become among the most invaded habitats globally. Ascidians are among the most notorious invaders in these ecosystems. Owing to their rapid spread, frequent population outbreaks, and associated negative ecological and economic impacts, invasive ascidians have become a global problem. Thus, the study of ascidian invasions has become a prominent area of invasion biology. Here, we review current knowledge and conclude that ascidians are good models for studying invasion success in the marine realm. Firstly, we summarize the reconstruction of invasion pathways or colonization histories and associated negative impacts of invasive ascidians, and address the urgent need to clarify ambiguous taxonomy of ascidians. Secondly, we discuss factors that underlie or facilitate invasion success of ascidians, including vectors of introduction and spread, environmental changes, biological traits, and possible genetic issues. Finally, we summarize current science-based policies and management solutions that are in place to prevent and control spread of invasive ascidians. We conclude by highlighting key research questions that remain to be answered, and propose future research to investigate mechanisms of invasion success in the marine realm using ascidians as model systems.

Supplementary material

227_2015_2734_MOESM1_ESM.pdf (42 kb)
Supplementary material 1 (PDF 42 kb)


  1. Adams CM, Shumway SE, Whitlatch RB, Chetchis T (2011) Biofouling in marine molluscan shellfish aquaculture: a survey assessing the business and economic implications of mitigation. J World Aquacult Soc 42:242–252CrossRefGoogle Scholar
  2. Airoldi L, Turon X, Perkol-Finkel S, Rius M (2015) Corridors for aliens but not for natives: effects of marine urban sprawl at a regional scale. Divers Distrib 21:755–768CrossRefGoogle Scholar
  3. Aldred N, Clare AS (2014) Impact and dynamics of surface fouling by solitary and compound ascidians. Biofouling 30:259–270CrossRefGoogle Scholar
  4. Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202CrossRefGoogle Scholar
  5. Australian Government (2011) Australian ballast water management requirements—version 5. Canberra, AustraliaGoogle Scholar
  6. Australian Government (2013) Anti-fouling and in-water cleaning guidelines. Canberra, AustraliaGoogle Scholar
  7. Ayre DJ, Davis AR, Billingham M, Llorens T, Styan C (1997) Genetic evidence for contrasting patterns of dispersal in solitary and colonial ascidians. Mar Biol 130:51–62CrossRefGoogle Scholar
  8. Baker HG, Stebbins GL (1965) The genetics of colonizing species. Academic Press, New York, NYGoogle Scholar
  9. Barrett SCH (2015) Foundations of invasion genetics: the Baker and Stebbins legacy. Mol Ecol 24:1927–1941CrossRefGoogle Scholar
  10. Beiras R, Fernández N, Bellas J, Besada V, González-Quijano A, Nunes T (2003) Integrative assessment of marine pollution in Galician estuaries using sediment chemistry, mussel bioaccumulation, and embryo-larval toxicity bioassays. Chemosphere 52:1209–1224CrossRefGoogle Scholar
  11. Ben-Shlomo R, Paz G, Rinkevich B (2006) Postglacial-period and recent invasions shape the population genetics of botryllid ascidians. Ecosystem 9:1118–1127CrossRefGoogle Scholar
  12. Ben-Shlomo R, Reem E, Douek J, Rinkevich B (2010) Population genetics of the invasive ascidian Botryllus schlosseri from South American coasts. Mar Ecol Prog Ser 412:85–92CrossRefGoogle Scholar
  13. Bernier RY, Locke A, Hanson JM (2009) Lobsters and crabs as potential vectors for tunicate dispersal in the southern Gulf of St. Lawrence, Canada. Aquat Invasions 4:105–110CrossRefGoogle Scholar
  14. Bingham BL, Young CM (1991) Larval behavior of the ascidian Ecteinascidia turbinata Herdman: an in situ experimental study of the effects of swimming on dispersal. J Exp Mar Biol Ecol 145:189–204CrossRefGoogle Scholar
  15. Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339CrossRefGoogle Scholar
  16. Blum JC, Chang AL, Liljesthröm M, Schenk ME, Steinberg MK, Ruiz GM (2007) The non-native solitary ascidian Ciona intestinalis (L.) depresses species richness. J Exp Mar Biol Ecol 342:5–14CrossRefGoogle Scholar
  17. Bock DG, Zhan A, Lejeusne C, MacIsaac HJ, Cristescu ME (2011) Looking at both sides of the invasion: patterns of colonization in the violet tunicate Botrylloides violaceus. Mol Ecol 20:503–516CrossRefGoogle Scholar
  18. Bock DG, MacIsaac HJ, Cristescu ME (2012) Multilocus genetic analyses differentiate between widespread and spatially restricted cryptic species in a model ascidian. Proc R Soc Lond B 279:2377–2385CrossRefGoogle Scholar
  19. Bock DG, Caseys C, Cousens RD, Hahn MA, Heredia SM, Hübner S, Turner KG, Whitney KD, Rieseberg LH (2015) What we still don’t know about invasion genetics. Mol Ecol 24:2277–2297CrossRefGoogle Scholar
  20. Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11CrossRefGoogle Scholar
  21. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115Google Scholar
  22. Briski E, Bailey SA, MacIsaac HJ (2011) Invertebrates and their dormant eggs transported in ballast sediments of ships arriving to the Canadian coasts and the Laurentian Great Lakes. Limnol Oceanogr 56:1929–1939CrossRefGoogle Scholar
  23. Briski E, Bailey SA, Casas-Monroy O, DiBacco C, Kaczmarska I, Lawrence JE, Leichsenring J, Levings C, MacGillivary ML, McKindsey CW, Nasmith LE, Parenteau M, Piercey GE, Rivkin RB, Rochon A, Roy S, Simard N, Sun B, Way C, Weise AM, MacIsaac HJ (2013) Taxon- and vector-specific variation in species richness and abundance during the transport stage of biological invasions. Limnol Oceanogr 58:1361–1372Google Scholar
  24. Brunetti R, Gissi C, Pennati R, Caicci F, Gasparini F, Manni L (2015) Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis. J Zool Syst Evol Res. doi:10.1111/jzs.12101 Google Scholar
  25. Buizer DAG (1980) Explosive development of Styela clava Herdman 1882, in the Netherlands after its introduction (Tunicata Ascidiacea). Bull Zool Mus 7:181–187Google Scholar
  26. Bullard SG, Carman MR (2009) Current trend in invasive ascidian research. In: Wilcox CP, Turpin RB (eds) Invasive species: detection, impact and control. Nova Science Publishers Inc, New York, NYGoogle Scholar
  27. 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 (2007a) 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
  28. Bullard SG, Sedlack B, Reinhardt JF, Litty C, Gareau K, Whitlatch RB (2007b) Fragmentation of colonial ascidians: differences in reattachment capability among species. J Exp Mar Biol Ecol 342:166–168CrossRefGoogle Scholar
  29. Cahil P, Heasman K, Jeffs A, Kuhajek J, Mountfort D (2012) Preventing ascidian fouling in aquaculture: screening selected allelochemicals for anti-metamorphic properties in ascidian larvae. Biofouling 28:39–49CrossRefGoogle Scholar
  30. Callahan AG, Deibel D, McKenzie CH, Hall JR, Rise ML (2010) Survey of harbours in Newfoundland for indigenous and non-indigenous ascidians and an analysis of their cytochrome c oxidase I gene sequences. Aquat Invasions 5:31–39CrossRefGoogle Scholar
  31. Caputi L, Andreakis N, Mastrototaro F, Cirino P, Vassillo M, Sordino P (2007) Cryptic speciation in a model invertebrate chordate. Proc Natl Acad Sci USA 104:9364–9369CrossRefGoogle Scholar
  32. 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
  33. Carlton JT, Gellar JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82CrossRefGoogle Scholar
  34. Carlton JT, Ruiz GM (2005) Vector science and integrated vector management in bioinvasion ecology: conceptual frameworks. In: Mooney HA, Mack RN, McNeely JA, Neville LE, Johan Schei P, Waage JK (eds) Invasive alien species: a new synthesis. Island Press, Covelo, CA, pp 36–58Google Scholar
  35. Carver CE, Chisholm A, Mallet AL (2003) Strategies to mitigate the impact of Ciona intestinalis (L.) biofouling on shellfish production. J Shellfish Res 22:621–631Google Scholar
  36. Carver CE, Mallet AL, Vercaemer B (2006) Biological synopsis of the colonial tunicates, Botryllus schlosseri and Botrylloides violaceus. Canadian Manuscript Report of Fisheries and Aquatic Sciences, vol 2747, p v + 42pGoogle Scholar
  37. Castilla JC, Guiňez 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 101:8517–8524CrossRefGoogle Scholar
  38. Chown SL, Hodgins KA, Griffin PC, Oakeshott JG, Byrne M, Hoffmann AA (2015) Biological invasions, climate change and genomics. Evol Appl 8:23–46CrossRefGoogle Scholar
  39. Chu KH, Tam PF, Fung CH, Chen QC (1997) A biological survey of ballast water in container ships entering Hong Kong. Hydrobiologia 352:201–206CrossRefGoogle Scholar
  40. Clancey L, Hinton R (2003) Distribution of the tunicate, Ciona intestinalis, in Nova Scotia. Nova Scotia Department of Fisheries and Agriculture, Nova ScotiaGoogle Scholar
  41. Cohen CS (1996) The effects of contrasting modes of fertilization on levels of inbreeding in the marine invertebrate genus Corella. Evolution 50:1896–1907CrossRefGoogle Scholar
  42. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558CrossRefGoogle Scholar
  43. Colautti RI, Bailey SA, van Overdijk CDA, Amundsen K, MacIsaac HJ (2006) Characterised and projected costs of nonindigenous species in Canada. Biol Invasions 8:45–59CrossRefGoogle Scholar
  44. Coutts ADM, Dodgshun TJ (2007) The nature and extent of organisms in vessel sea-chests: a protected mechanism for marine bioinvasions. Mar Pollut Bull 54:875–886CrossRefGoogle Scholar
  45. Coutts ADM, Forrest BM (2007) Development and application of tools for incursion response: lessons learned from the management of the fouling pest Didemnum vexillum. J Exp Mar Biol Ecol 342:154–162CrossRefGoogle Scholar
  46. Coutts ADM, Moore KM, Hewitt CL (2003) Ships’ sea-chests: an overlooked transfer mechanism for non-indigenous marine species? Mar Pollut Bull 46:1504–1515CrossRefGoogle Scholar
  47. Coutts ADM, Piola RF, Hewitt CL, Connell SD, Gardner JPA (2010) Effect of vessel voyage speed on survival of biofouling organisms: implications for translocation of non-indigenous marine species. Biofouling 26:1–13CrossRefGoogle Scholar
  48. Crawford KM, Whitney KD (2010) Population genetic diversity influences colonization success. Mol Ecol 19:1253–1263CrossRefGoogle Scholar
  49. Darbyson E, Locke A, Hanson JM, Willison HM (2009a) Marine boating habits and the potential for spread of invasive species in the Gulf of St. Lawrence. Aquat Invasions 4:87–94CrossRefGoogle Scholar
  50. Darbyson E, Hanson JM, Locke A, Willison HM (2009b) Settlement and potential for transport of clubbed tunicate (Styela clava) on boat hulls. Aquat Invasions 4:95–103CrossRefGoogle Scholar
  51. Darling JA, Herborg L, Davidson I (2012) Intracoastal shipping drives patterns of regional population expansion by an invasive marine invertebrate. Ecol Evol 2:2557–2566CrossRefGoogle Scholar
  52. David GK, Marshall DJ, Riginos C (2010) Latitudinal variability in spatial genetic structure in the invasive ascidian, Styela plicata. Mar Biol 157:1955–1965CrossRefGoogle Scholar
  53. Davis MH, Davis ME (2004) The distribution limits of Styela clava (Tunicata, Ascidiacea) in European waters. Porcup Mar Nat Hist Soc Newsl 15:35–43Google Scholar
  54. Davis MH, Davis ME (2008) First record of Styela clava (Tunicata, Ascidiacea) in the Mediterranean region. Aquat Invasions 3:125–132CrossRefGoogle Scholar
  55. De Silva SS, Nguyen TTT, Turchini GM, Amarasinghe US, Abery NW (2009) Alien species in aquaculture and biodiversity: a paradox in food production. Ambio 38:24–28CrossRefGoogle Scholar
  56. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167CrossRefGoogle Scholar
  57. Department of Fisheries, Aquaculture and Rural Development (2012) Annual Report 2010–2011. Prince Edward Island, CanadaGoogle Scholar
  58. Department of Fisheries, Aquaculture and Rural Development (2014) Annual Report 2012–2013. Prince Edward Island, CanadaGoogle Scholar
  59. Department of Fisheries and Oceans Canada (2005) Governments of Canada and PEI announce funding for invasive tunicates. Fisheries and Oceans Canada, Media Room, News ReleaseGoogle Scholar
  60. Dijkstra J, Harris LG, Westerman E (2007) Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine. J Exp Mar Biol Ecol 342:61–68CrossRefGoogle Scholar
  61. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449CrossRefGoogle Scholar
  62. 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. Divers Distrib 13:808–817CrossRefGoogle Scholar
  63. 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 southwest England, 50 years after its introduction. Mol Ecol 18:442–453CrossRefGoogle Scholar
  64. Dupont L, Viard F, Davis MH, Nishikawa T, Bishop JDD (2010) Pathways of spread of the introduced ascidian Styela clava (Tunicata) in Northern Europe, as revealed by microsatellite markers. Biol Invasions 12:2707–2721CrossRefGoogle Scholar
  65. Dybern BI (1965) The life cycle of Ciona intestinalis (L.) f. typica in the relation to environmental temperature. Oikos 16:109–131CrossRefGoogle Scholar
  66. Dybern BI (1967) Settlement of sessile animals on eternite slabs in two polls near Bergen. Sarsia 29:137–180CrossRefGoogle Scholar
  67. Egan SP, Barnes MA, Hwang C, Mahon AR, Feder JL, Ruggiero ST, Tanner CE, Lodge DM (2013) Rapid invasive species detection by combining environmental DNA with light transmission spectroscopy. Conserv Lett 6:402–409CrossRefGoogle Scholar
  68. Ellstrand NC, Schierenbeck K (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050CrossRefGoogle Scholar
  69. Epelbaum A, Herborg JM, Therriault TW, Pearce CM (2009) Temperature and salinity effects on growth, survival, reproduction, and potential distribution of two non-indigenous botryllid ascidians in British Columbia. J Exp Mar Biol Ecol 369:43–52CrossRefGoogle Scholar
  70. Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130CrossRefGoogle Scholar
  71. Fautin D, Dalton P, Incze LS, Leong J-AC, Pautzke C, Rosenberg A, Sandifer P, Sedberry G, Tunnell JW, Abbott I, Brainard RE, Brodeur M, Eldredge LG, Feldman M, Moretzsohn F, Vroom PS, Wainstein M, Wolff N (2010) An overview of marine biodiversity in United States waters. PLoS One 5:e11914CrossRefGoogle Scholar
  72. Fay RC, Johnson JV (1971) Observations on the distribution and ecology of the littoral ascidians of the mainland coast of Southern California. Bull South Calif Acad Sci 70:114–124Google Scholar
  73. Fitridge I, Dempster T, Guenther J, de Nys R (2012) The impact and control of biofouling in marine aquaculture: a review. Biofouling 28:649–669CrossRefGoogle Scholar
  74. Fletcher LM, Forrest BM, Bell JJ (2013) Impacts of the invasive ascidian Didemnum vexillum on green-lipped mussel Perna canaliculus aquaculture in New Zealand. Aquacult Environ Interact 4:17–30CrossRefGoogle Scholar
  75. Gab-Alla AAFA (2008) Distribution of the sea squirt Ecteinascidia thurstoni Herdman, 1890 (Ascidiacea: Perophoridae) along Suez Canal and Egyptian Red Sea Coasts. Oceanologia 50:239–253Google Scholar
  76. Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Annu Rev Mar Sci 2:367–393CrossRefGoogle Scholar
  77. Gittenberger A (2007) Recent population expansions of nonnative ascidians in the Netherlands. J Exp Mar Biol Ecol 342:122–126CrossRefGoogle Scholar
  78. Gittenberger A (2009) Invasive tunicates on Zeeland and Prince Edward Island mussels, and management practices in the Netherlands. Aquat Invasions 4:279–281CrossRefGoogle Scholar
  79. Godwin LS (2003) Hull fouling of maritime vessels as a pathway for marine species invasions to the Hawaiian Islands. Biofouling 19:123–131CrossRefGoogle Scholar
  80. Goldstien SJ, Schiek DR, Gemmell NJ (2010) Regional connectivity and coastal expansion: differentiating preborder and post-border vectors for the invasive tunicate Styela clava. Mol Ecol 19:874–885CrossRefGoogle Scholar
  81. Goldstien SJ, Dupont L, Viard F, Hallas PJ, Nishikawa T, Schiel DR, Gemmell NJ, Bishop JDD (2011) Global phylogeography of the widely introduced north pacific ascidian Styela clava. PLoS One 6:e16755CrossRefGoogle Scholar
  82. Government of Canada (2006) Ballast water control and management regulations. Canada Gazette 140(l3), OttawaGoogle Scholar
  83. Grey EK (2009) Do we need to jump in? A comparison of two survey methods of exotic ascidians on docks. Aquat Invasions 4:81–86CrossRefGoogle Scholar
  84. Haydar D, Hoarau G, Olsen JL, Stam WT, Wolff WJ (2011) Introduced or glacial relict? Phylogeography of the cryptogenic tunicate Molgula manhattensis (Ascidiacea, Pleurogona). Divers Distrib 17:68–80CrossRefGoogle Scholar
  85. Helyar SJ, Hemmer-Hansen J, Bekkevold D, Taylor MI, Ogden R, Limborg MT, Cariani A, Maes GE, Dopere E, Carvalho GR, Nielsen EE (2011) Application of SNPs for population genetics of nonmodel organisms: new opportunities and challenges. Mol Ecol Resour 11:123–136CrossRefGoogle Scholar
  86. Herborg L-M, O’Hara P, Therriault TW (2009) Forecasting the potential distribution of the invasive tunicate Didemnum vexillum. J Appl Ecol 46:64–72CrossRefGoogle Scholar
  87. Holloway MG, Connell SD (2002) Why do floating structures create novel habitats for subtidal epibiota? Mar Ecol Prog Ser 235:43–52CrossRefGoogle Scholar
  88. Hulme PE, Bacher S, Kenis M, Klotz S, Kühn I, Minchin D, Nentwig W, Olenin S, Panov V, Pergl J, Pyšek P, Roques A, Sol D, Solarz W, Vilà M (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol 45:403–414CrossRefGoogle Scholar
  89. International Maritime Organization (IMO) (2004) International convention for the control and management of ships’ ballast water and sediments, LondonGoogle Scholar
  90. International Maritime Organization (IMO) (2011) Guidelines for the control and management of ships’ biofouling to minimize the transfer of invasive species, London Google Scholar
  91. Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181CrossRefGoogle Scholar
  92. Lacoursiere-Roussel A, Bock DG, Cristescu ME, Guichard F, Girard P, Legendre P, McKindsey CW (2012) Disentangling invasion processes in a dynamic shipping-boating network. Mol Ecol 21:4227–4241CrossRefGoogle Scholar
  93. Lahille F (1886) Sur la classification des Tuniciers. CR Acad Sci Paris 102:1573–1575Google Scholar
  94. Lambert G (2003) Marine biodiversity of Guam: the Ascidiacea. Micronesica 35–36:584–593Google Scholar
  95. Lambert G (2004) The south temperate and Antarctic ascidian Corella eumyota reported in two harbours in north-western France. J Mar Biol Assoc UK 84:239–241CrossRefGoogle Scholar
  96. Lambert G (2005) Ecology and natural history of the protochordates. Can J Zool 83:34–50CrossRefGoogle Scholar
  97. Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4CrossRefGoogle Scholar
  98. 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
  99. Lambert CC, Lambert G (1998) Nonindigenous ascidians in southern California harbors and marinas. Mar Biol 130:675–688CrossRefGoogle Scholar
  100. 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
  101. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  102. Lee CE, Kiergaard M, Eads BD, Gelembiuk GW, Posavi M (2011) Pumping ions: rapid parallel evolution of ionic regulation following habitat invasions. Evolution 65:2229–2244CrossRefGoogle Scholar
  103. Lejeusne C, Bock DG, Therriault TW, MacIsaac HJ, Cristescu ME (2011) Comparative phylogeography of two colonial ascidians reveals contrasting invasion histories in North America. Biol Invasions 13:635–650CrossRefGoogle Scholar
  104. Lengyel NL, Collie JS, Valentine PC (2009) The invasive colonial ascidian Didemnum vexillum on Georges Bank—ecological effects and genetic identification. Aquat Invasions 4:143–152CrossRefGoogle Scholar
  105. Leung B, Lodge DM, Finnoff D, Shogren JF, Lewis MA, Lamberti G (2002) An ounce of prevention or a pound of cure: bioeconomic risk analysis of invasive species. Proc R Soc Lond B 269:2407–2413CrossRefGoogle Scholar
  106. Levings C, Kieser D, Jamieson G, Dudas S (2002) Marine and estuarine alien species in the Strait of Georgia, British Columbia. In: Claudi R (ed) Alien species in Canada. Natural Resources Canada, Ottawa, pp 111–131Google Scholar
  107. Lin Y, Gao Z, Zhan A (2015) Introduction and use of non-native species for aquaculture in China: status, risks and management solutions. Rev Aquacult 7:28–58CrossRefGoogle Scholar
  108. Locke A (2009) A screening procedure for potential tunicate invaders of Atlantic Canada. Aquat Invasions 4:71–79CrossRefGoogle Scholar
  109. Locke A, Hanson JM (2009a) Rapid response to non-indigenous species. 3. A proposed framework. Aquat Invasions 4:259–273CrossRefGoogle Scholar
  110. Locke A, Hanson JM (2009b) Rapid response to non-indigenous species. 1. Goals and history of rapid response in the marine environment. Aquat Invasions 4:237–247CrossRefGoogle Scholar
  111. 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 342:69–77CrossRefGoogle Scholar
  112. Locke A, Hanson JM, MacNair NG, Smith AH (2009) Rapid response to non-indigenous species. 2. Case studies of invasive tunicates in Prince Edward Island. Aquat Invasions 4:249–258CrossRefGoogle Scholar
  113. Lodge DM, Williams S, MacIsaac 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
  114. Lodge DM, Turner CR, Jerde CL, Barnes MA, Chadderton L, Egan SP, Feder JL, Mahon AR, Pfrender ME (2012) Conservation in a cup of water: estimating biodiversity and population abundance from environmental DNA. Mol Ecol 21:2555–2558CrossRefGoogle Scholar
  115. López-Legentil S, Turon X, Planes S (2006) Genetic structure of the star sea squirt, Botryllus schlosseri, introduced in southern European harbours. Mol Ecol 15:3957–3967CrossRefGoogle Scholar
  116. Lutz-Collins V, Ramsay A, Quijón PA, Davidson J (2009) Invasive tunicates fouling mussel lines: evidence of their impact on native tunicates and other epifaunal invertebrates. Aquat Invasions 4:213–220CrossRefGoogle Scholar
  117. Marshall DJ, Keough MJ (2003) Variation in the dispersal potential of non-feeding invertebrate larvae: the desperate larva hypothesis and larval size. Mar Ecol Prog Ser 255:145–153CrossRefGoogle Scholar
  118. McEnnulty FR, Bax NJ, Schaffelke B, Campbell ML (2001) A review of rapid response options for the control of ABWMAC listed introduced marine pest species and related taxa in Australian waters. Centre for Research on Introduced Marine Pests Technical Report 23. CSIRO Marine Research, Hobart, AustraliaGoogle Scholar
  119. McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291CrossRefGoogle Scholar
  120. McKindsey CW, Landry T, O’Beirn FX, Davies IM (2007) Bivalve aquaculture and exotic species: a review of ecological considerations and management issues. J Shellfish Res 26:281–294CrossRefGoogle Scholar
  121. Mead A, Carlton JT, Griffiths CL, Rius M (2011) Introduced and cryptogenic marine and estuarine species of South Africa. J Nat Hist 45:2463–2524CrossRefGoogle Scholar
  122. Mercer JM, Whitlatch RB, Osman RW (2009) Potential effects of the invasive colonial ascidian (Didemnum vexillum Kott, 2002) on peddle-cobble bottom habitats in Long Island Sound, USA. Aquat Invasions 4:133–142CrossRefGoogle Scholar
  123. Milkman R (1967) Genetic and developmental studies on Botryllus schlosseri. Biol Bull 132:229–243CrossRefGoogle Scholar
  124. Minchin D (2007) Rapid coastal survey for targeted alien species associated with floating pontoons in Ireland. Aquat Invasions 1:143–147CrossRefGoogle Scholar
  125. Minchin D, Davis MH, Davis ME (2006) Spread of the Asian tunicate Styela clava Herdman, 1882 to the east and south-west of Ireland. Aquat Invasions 1:91–96CrossRefGoogle Scholar
  126. Monniot C, Monniot F, Laboute P (1991) Coral reef ascidians of New Caledonia. ORSTOM, ParisGoogle Scholar
  127. Muirhead JR, Gray DK, Kelly DW, Ellis SM, Heath DD, MacIsaac HJ (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:431–449CrossRefGoogle Scholar
  128. Muñoz J, McDonald J (2014) Potential Eradication and Control Methods for the Management of the Ascidian Didemnum perlucidum in Western Australia. Fisheries Research Report No. 252Google Scholar
  129. Murray CC, Pakhomov EA, Therriault TW (2011) Recreational boating: a large unregulated vector transporting marine invasive species. Divers Distrib 17:1161–1172CrossRefGoogle Scholar
  130. Naranjo SA, Carballo JL, Garcia-Gomez JC (1996) Effects of environmental stress on ascidian populations in Algeciras Bay (southern Spain). Possible marine bioindicators? Mar Ecol Prog Ser 144:119–131CrossRefGoogle Scholar
  131. Naylor RL, Williams SL, Strong DR (2001) Aquaculture—a gateway for exotic species. Science 294:1655–1656CrossRefGoogle Scholar
  132. New Zealand Government (2010) Requirements for Vessels Arriving in New Zealand. Ministry for Primary Industries, WellingtonGoogle Scholar
  133. Nomaguchi TA, Nishijima C, Minowa S, Hashimoto M, Haraguchi C, Amemiya S, Fujisawa H (1997) Embryonic thermosensitivity of the ascidian, Ciona savignyi. Zool Sci 14:511–515CrossRefGoogle Scholar
  134. Nydam ML, Harrison RG (2007) Genealogical relationships within and among shallow-water Ciona species (Ascidiacea). Mar Biol 151:1839–1847CrossRefGoogle Scholar
  135. Nydam ML, Harrison RG (2010) Polymorphism and divergence within the ascidian genus Ciona. Mol Phylogent Evol 56:718–726CrossRefGoogle Scholar
  136. Ordoñez V, Pascual M, Rius M, Turon X (2013) Mixed but not admixed: a spatial analysis of genetic variation of an invasive ascidian on natural and artificial substrates. Mar Biol 160:1645–1660CrossRefGoogle Scholar
  137. Ordoñez V, Pascual M, Fernández-Tejedor 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 17:2075–2085CrossRefGoogle Scholar
  138. Pérez-Portela R, Bishop JDD, Davis AR, Turon X (2009) Phylogeny of the families Pyuridae and Styelidae (Stolidobranchiata, Ascidiacea) inferred from mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 50:560–570CrossRefGoogle Scholar
  139. Pérez-Portela R, Turon X, Bishop JDD (2012) Bottlenecks and loss of genetic diversity: spatio-temporal patterns of genetic structure in an ascidian recently introduced in Europe. Mar Ecol Prog Ser 451:93–105CrossRefGoogle Scholar
  140. Pérez-Portela R, Arranz V, Rius M, Turon X (2013) Cryptic speciation or global spread? The case of a cosmopolitan marine invertebrate with limited dispersal capabilities. Sci Rep 3:3197Google Scholar
  141. Petersen JK (2007) Ascidian suspension feeding. J Exp Mar Biol Ecol 342:127–137CrossRefGoogle Scholar
  142. Pineda MC, López-Legentil S, Turon X (2011) The whereabouts of an ancient wanderer: global phylogeography of the solitary ascidian Styela plicata. PLoS One 6:e25495CrossRefGoogle Scholar
  143. 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:e46672CrossRefGoogle Scholar
  144. Pisut DP, Pawlik JR (2002) Anti-predatory chemical defenses of ascidians: secondary metabolites or inorganic acids? J Exp Mar Biol Ecol 270:203–214CrossRefGoogle Scholar
  145. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294CrossRefGoogle Scholar
  146. Procaccini G, Affinito O, Toscano F, Sordino P (2011) A new animal model for merging ecology and evolution. In: Pontarotti P (ed) Evolutionary biology—concepts, biodiversity, macroevolution and genome evolution. Springer, Berlin, pp 91–106CrossRefGoogle Scholar
  147. Ramsay A, Davidson J, Landry T, Arsenault G (2008) Process of invasiveness among exotic tunicates in Prince Edward Island, Canada. Biol Invasions 10:1311–1316CrossRefGoogle Scholar
  148. Reaser JK, Meyerson LA, Von Holle B (2008) Saving camels from straws: how propagule pressure-based prevention policies can reduce the risk of biological invasion. Biol Invasions 10:1085–1098CrossRefGoogle Scholar
  149. Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evol Int J Org Evol 55:1095–1103CrossRefGoogle Scholar
  150. Reem E, Douek J, Katzir G, Rinkevich B (2013) Long-term population genetic structure of an invasive urochordate: the ascidian Botryllus schlosseri. Biol Invasions 15:225–241CrossRefGoogle Scholar
  151. Rhyne AL, Tlusty MF, Schofield PJ, Kaufman L, Morris JA Jr, Bruckner AW (2012) Revealing the appetite of the marine aquarium fish trade: the volume and biodiversity of fish imported into the United States. PLoS One 7:e35808CrossRefGoogle Scholar
  152. Ricciardi A, Rasmussen JB (1998) Predicting the identity and impact of future biological invaders: a priority for aquatic resource management. Can J Fish Aquat Sci 55:1759–1765CrossRefGoogle Scholar
  153. Rilov G, Crooks JA (2009) Marine bioinvasions: conservation hazards and vehicles for ecological understanding. In: Rilov G, Crooks JA, Jeffrey A (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 1–9CrossRefGoogle Scholar
  154. Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242CrossRefGoogle Scholar
  155. Rius M, Shenkar N (2012) Ascidian introductions through the Suez Canal: the case study of an Indo-Pacific species. Mar Pollut Bull 64:2060–2068CrossRefGoogle Scholar
  156. 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 14:818–828CrossRefGoogle Scholar
  157. Rius M, Pineda MC, Turon X (2009) Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea. Biol Invasions 11:2181–2194CrossRefGoogle Scholar
  158. Rius M, Heasman KG, McQuaid CD (2011) Long-term coexistence of non-indigenous species in aquaculture facilities. Mar Pollut Bull 62:2395–2403CrossRefGoogle Scholar
  159. Rius M, Turon X, Ordóñez V, Pascual M (2012) Tracking invasion histories in the sea: facing complex scenarios using multilocus data. PLoS One 7:e35815CrossRefGoogle Scholar
  160. Rius M, Clusella-Trullas S, McQuaid CD, Navarro RA, Griffiths CL, Matthee CA, von der Heyden S, Turon X (2014a) Range expansions across ecoregions: interactions of climate changes, physiology and genetic diversity. Glob Ecol Biogeogr 23:76–88CrossRefGoogle Scholar
  161. Rius M, Potter EE, Aguirre JD, Stachowicz JJ (2014b) Mechanisms of biotic resistance across complex life cycles. J Anim Ecol 83:296–305CrossRefGoogle Scholar
  162. Rius M, Bourne S, Hornsby HG, Chapman MA (2015a) Applications of next-generation sequencing to the study of biological invasions. Curr Zool 61:488–504CrossRefGoogle Scholar
  163. Rius M, Turon X, Bernardi G, Volckaert FAM, Viard F (2015b) Marine invasion genetics: from spatio-temporal patterns to evolutionary outcomes. Biol Invasions 17:869–885CrossRefGoogle Scholar
  164. Robinson TB, Griffiths CL, McQuaid CD, Rius M (2005) Marine alien species of South Africa—status and impacts. Afr J Mar Sci 27:297–306CrossRefGoogle Scholar
  165. Rocha RM (2002) Bostricobranchus digonas Abbott (Ascidiacea, Molgulidae) in Paranaguá Bay, Paraná, Brazil. A case of recent invasion? Rev Bras Zool 19:157–161Google Scholar
  166. Rodriguez LF, Ibarra-Obando SE (2008) Cover and colonization of commercial oyster (Crassostrea gigas) shells by fouling organisms in San Quintin Bay, Mexico. J Shellfish Res 27:337–343CrossRefGoogle Scholar
  167. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464CrossRefGoogle Scholar
  168. Ruiz GM, Carlton JT (2003) Invasion vectors: a conceptual framework for management. In: Ruiz GM, Carlton JT (eds) Invasive species: vectors and management strategies. Island Press, Washington, pp 459–504Google Scholar
  169. Sephton D, Vercaemer B, Nicolas JM, Keays J (2011) Monitoring for invasive tunicates in Nova Scotia, Canada (2006–2009). Aquat Invasions 6:391–403CrossRefGoogle Scholar
  170. Shenkar N, Swalla BJ (2011) Global diversity of Ascidiacea. PLoS One 6:e20657CrossRefGoogle Scholar
  171. Shenkar N, Zeldman Y, Loya Y (2008) Ascidian recruitment patterns on an artificial reef in Eilat (Red Sea). Biofouling 24:119–128CrossRefGoogle Scholar
  172. Simkanin C, Davidson IC, Dower JF, Jamieson G, Therriault TW (2012) Anthropogenic structures and the infiltration of natural benthos by invasive ascidians. Mar Ecol 33:499–511CrossRefGoogle Scholar
  173. Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002) Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83:2575–2590CrossRefGoogle Scholar
  174. Stefaniak L, Lambert G, Gittenberger A, Zhang H, Lin S, Whitlatch RB (2009) Genetic conspecificity of the worldwide populations of Didemnum vexillum Kott, 2002. Aquat Invasions 4:29–44CrossRefGoogle Scholar
  175. Stoner DS, Ben-shlomo 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 243:93–100CrossRefGoogle Scholar
  176. Svane I, Young CM (1989) The ecology and behaviour of ascidian larvae. Oceanogr Mar Biol Annu Rev 27:45–90Google Scholar
  177. Sylvester F, Kalaci O, Leung B, Lacoursière-Roussel A, Murray CC, Choi FM, Bravo MA, Therriault TW, MacIsaac HJ (2011) Hull fouling as an invasion vector: Can simple models explain a complex problem? J Appl Ecol 48:415–423CrossRefGoogle Scholar
  178. Teske PR (2014) Connectivity in solitary ascidians: Is a 24-h propagule duration sufficient to maintain large-scale genetic homogeneity? Mar Biol 161:2681–2687CrossRefGoogle Scholar
  179. Teske PR, Sandoval-Castillo J, Waters JM, Beheregaray LB (2014) Can novel genetic analyses help to identify low-dispersal marine invasive species? Ecol Evol 4:2848–2886CrossRefGoogle Scholar
  180. Therriault TW, Herborg LM (2008) Predicting the potential distribution of the vase tunicate Ciona intestinalis in Canadian waters: informing a risk assessment. ICES J Mar Sci 65:788–794CrossRefGoogle Scholar
  181. Thomsen PF, Kielgast J, Iversen LL, Wiuf C, Rasmussen M, Gilbert MT, Orlando L, Willerslev E (2012) Monitoring endangered freshwater biodiversity using environmental DNA. Mol Ecol 21:2565–2573CrossRefGoogle Scholar
  182. Tsagkogeorga G, Turon X, Hopcroft RR, Tilak M, Feldstein T, Shenkar N, Loya Y, Huchon D, Douzery EJP, Delsuc F (2009) An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models. BMC Evol Biol 9:187CrossRefGoogle Scholar
  183. Turon X, Tarjuelo I, Duran S, Pasucal M (2003) Characterising invasion processes with genetic data: an Atlantic clade of Clavelina lepadiformis (Ascidiacea) introduced into Mediterranean harbours. Hydrobiologia 503:29–35CrossRefGoogle Scholar
  184. Turon X, Nishikawa T, Rius M (2007) Spread of Microcosmus squamiger (Ascidiacea: Pyuridae) in the Mediterranean Sea and adjacent waters. J Exp Mar Biol Ecol 342:185–188CrossRefGoogle Scholar
  185. United States Coast Guard (USCG) (1993) Ballast water management for vessels entering the Great Lakes. Code of Federal Regulations 33-CFR Part 151.1510Google Scholar
  186. Valentine PC, Carman MR, Blackwood DS, Heffron EJ (2007) Ecological observations on the colonial ascidian Didemnum sp. in a new England tide pool habitat. J Exp Mar Biol Ecol 32:109–121CrossRefGoogle Scholar
  187. van Name WG (1945) The North and South American Ascidians. Bull Am Nat Hist 84:1–463Google Scholar
  188. Vandepitte K, de Meyer T, Helsen K, van Acker K, Roldán-Ruiz I, Mergeay J, Honnay O (2014) Rapid genetic adaptation precedes the spread of an exotic plant species. Mol Ecol 23:2157–2164CrossRefGoogle Scholar
  189. Voskoboynik A, Neff NF, Sahoo D, Newman AM, Pushkarev D, Koh W, Passarelli B, Fan HC, Mantalas G, Palmeri KJ, Ishizuka KJ, Gissi C, Griggio F, Ben-shlomo R, Corey DM, Penland L, White RA III, Weissman IR, Quake SR (2013) The genome sequence of the colonial chordate, Botryllus schlosseri. Elife 2:e00569CrossRefGoogle Scholar
  190. Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24:136–144CrossRefGoogle Scholar
  191. Wonham M, Carlton J (2005) Cool-temperate marine invasions at local and regional scales: the Northeast Pacific Ocean as a model system. Biol Invasions 7:369–392CrossRefGoogle Scholar
  192. Wotton DM, Hewitt CL (2004) Marine biosecurity postborder management: developing incursion response systems for New Zealand. N Z J Mar Fresh 38:553–555CrossRefGoogle Scholar
  193. Yamaguchi M (1975) Growth and reproductive cycles of the marine fouling ascidians Ciona intestinalis, Styela plicata, Botrylloides violaceus, and Leptoclinum mitsukurii at Aburatsubo-Moroiso Inlet (Central Japan). Mar Biol 29:253–259CrossRefGoogle Scholar
  194. Zaniolo G, Manni L, Brunetti R, Burighel P (1998) Brood pouch differentiation in Botrylloides violaceus, a viviparous ascidian (Tunicata). Invertebr Reprod Dev 33:11–24CrossRefGoogle Scholar
  195. Zhan A, MacIsaac HJ (2015) Rare biosphere exploration using high-throughput sequencing: research progress and perspective. Conserv Genet 16:513–522CrossRefGoogle Scholar
  196. Zhan A, MacIsaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol 19:4678–4694CrossRefGoogle Scholar
  197. Zhan A, Darling JA, Bock DG, Lacoursière-Roussel A, MacIsaac HJ, Cristescu ME (2012) Complex genetic patterns in closely related colonizing invasive species. Ecol Evol 2:1331–1346CrossRefGoogle Scholar
  198. Zhan A, Hulák M, Sylvester F, Huang X, Adebayo AA, Abbott CL, Adamowicz SJ, Heath DD, Cristescu ME, MacIsaac HJ (2013) High sensitivity of 454 pyrosequencing for detection of rare species in aquatic communities. Methods Ecol Evol 4:558–565CrossRefGoogle Scholar
  199. Zhan A, Bailey SA, Heath DD, MacIsaac HJ (2014a) Performance comparison of genetic markers for high-throughput sequencing-based biodiversity assessment in complex communities. Mol Ecol Resour 14:1049–1059Google Scholar
  200. Zhan A, He S, Brown EA, Chain FJJ, Therriault TW, Abbott CL, Heath DD, Cristescu ME, MacIsaac HJ (2014b) Reproducibility of pyrosequencing data for biodiversity assessment in complex communities. Methods Ecol Evol 5:881–890CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Aibin Zhan
    • 1
  • Elizabeta Briski
    • 2
  • Dan G. Bock
    • 3
  • Sara Ghabooli
    • 4
  • Hugh J. MacIsaac
    • 4
  1. 1.Research Center for Eco-Environmental SciencesChinese Academy of SciencesBeijingChina
  2. 2.Experimental EcologyHelmholtz Centre for Ocean ResearchKielGermany
  3. 3.Department of Botany, Biodiversity Research CentreUniversity of British ColumbiaVancouverCanada
  4. 4.Great Lakes Institute for Environmental ResearchUniversity of WindsorWindsorCanada

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