Skip to main content
Log in

Year-round reproduction in a seasonal sea: biological cycle of the introduced ascidian Styela plicata in the Western Mediterranean

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The widely introduced ascidian Styela plicata is very common in the Western Mediterranean, an area that can act as a source for secondary introductions due to its high shipping activity. In order to understand the potential of this species to colonize new habitats, its reproductive features were assessed in the Western Mediterranean by means of monthly monitoring of two populations (Vilanova i la Geltrú 41°12′53″N, 1°44′11″E; Blanes 41°40′29″N, 2°47′56″E) from January 2009 to December 2010. The reproductive activity of this species was assessed through gonad histology and a gonad index. Population size-structure was measured monthly in order to study recruitment dynamics. No clear seasonal pattern was observed, and mature gametes and recruits were present all year long. Spawning was potentially continuous, although it seemed punctuated with pulses of gamete release, particularly in spring. A prolonged reproductive period is likely to confer a competitive advantage on S. plicata in temperate seas, where most species reproduce seasonally, and may promote recurrent introductions as larvae are available for settlement on transport vectors over much of the year.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Agius BP (2007) Spatial and temporal effects of pre-seeding plates with invasive ascidians: growth, recruitment and community composition. J Exp Mar Biol Ecol 342:30–39

    Article  Google Scholar 

  • Allen F (1953) Distribution of marine invertebrates by ships. Aust J Mar Freshw Res 4:307–316

    Article  Google Scholar 

  • Altman S, Whitlatch RB (2007) Effects of small-scale disturbance on invasion success in marine communities. J Exp Mar Biol Ecol 342:15–29

    Article  Google Scholar 

  • Ballesteros E (1989) Production of seaweeds in Northwestern Mediterranean marine communities: its relation with environmental factors. Sci Mar 53:357–364

    Google Scholar 

  • Barros R, Rocha R, Pie M (2009) Human-mediated global dispersion of Styela plicata (Tunicata, Ascidiacea). Aquatic Inv 4:45–57

    Article  Google Scholar 

  • Becerro MA, Turon X (1992) Reproductive cycles of the ascidians Microcosmus sabatieri and Halocynthia papillosa in the Northwestern Mediterranean. Mar Ecol 13:363–373

    Article  Google Scholar 

  • Bingham BL (1997) Light cycles and gametogenesis in three temperate ascidian species. Invertebr Biol 116:61–70

    Article  Google Scholar 

  • Blackburn TM, Duncan RP (2001) Determinants of establishment success in introduced birds. Nature 414:195–197

    Article  CAS  Google Scholar 

  • Blakeslee AMH, McKenzie CH, Darling JA, Byers JE, Pringle JM, Roman J (2010) A hitchhiker’s guide to the Maritimes: anthropogenic transport facilitates long-distance dispersal of an invasive marine crab to Newfoundland. Divers Distrib 16:879–891

    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 

  • Carlton JT (1989) Mans 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 (2009) Deep invasion ecology and the assembly of communities in historical time. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 13–56

    Chapter  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, 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  Google Scholar 

  • Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110

    Article  Google Scholar 

  • Coma R, Ribes M, Gili JM, Zabala M (2000) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453

    Article  Google Scholar 

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

    Article  Google Scholar 

  • David GK, Marshall DJ, Riginos C (2010) Latitudinal variability in spatial genetic structure in the invasive ascidian, Styela plicata. Mar Biol 157:1955–1965

    Article  Google Scholar 

  • 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 244:125–137

    Article  Google Scholar 

  • Fine M, Zibrowius H, Loya Y (2001) Oculina patagonica: a non-lessepsian scleractinian coral invading the Mediterranean Sea. Mar Biol 138:1195–1203

    Article  Google Scholar 

  • Floerl O, Inglis GJ (2005) Starting the invasion pathway: the interaction between source populations and human transport vectors. Biol Invasions 7:589–606

    Article  Google Scholar 

  • Fowler AE, Gerner NV, Sewell MA (2011) Temperature and salinity tolerances of Stage 1 zoeae predict possible range expansion of an introduced portunid crab, Charybdis japonica, in New Zealand. Biol Invasions 13:691–699

    Article  Google Scholar 

  • Glasby TM (2001) Development of sessile marine assemblages on fixed versus moving substrata. Mar Ecol Prog Ser 215:37–47

    Article  Google Scholar 

  • Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27

    Article  Google Scholar 

  • Grosholz ED, Ruiz GM (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas. Biol Conserv 78:59–66

    Article  Google Scholar 

  • Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion—implications for conservation. Conserv Biol 6:324–337

    Article  Google Scholar 

  • King CK, Hoegh-Guldberg O, Byrne M (1994) Reproductive cycle of Centrostephanus rodgersii (Echinoidea), with recommendations for the establishment of a sea urchin fishery in New South Wales. Mar Biol 120:95–106

    Google Scholar 

  • Lambert G (2002) Nonindigenous ascidians in tropical waters. Pac Sci 56:291–298

    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 (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 

  • 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 296:219–228

    Article  Google Scholar 

  • Lozano J, Galera J, López S, Turon X, Palacín C, Morera G (1995) Biological cycles and recruitment of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Mar Ecol Prog Ser 122:179–191

    Article  Google Scholar 

  • Mack MC, D’Antonio CM (1998) Impacts of biological invasions on disturbance regimes. Trends Ecol Evol 13:195–198

    Article  CAS  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Marchetti MP, Moyle PB, Levine R (2004) Alien fishes in California watersheds: characteristics of successful and failed invaders. Ecol Appl 14:587–596

    Article  Google Scholar 

  • Margalef R (1985) Key environments: Western Mediterranean. Pergamon Press, New York

    Google Scholar 

  • McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890

    Article  Google Scholar 

  • McMahon RF (1996) The physiological ecology of the zebra mussel, Dreissena polymorpha, in North America and Europe. Am Zool 36:339–363

    Google Scholar 

  • Millar RH (1971) The biology of ascidians. Adv Mar Biol 9:1–100

    Article  Google Scholar 

  • Nandakumar K, Tanaka M, Kikuchi T (1993) Interspecific competition among fouling organisms in Tomioka Bay, Japan. Mar Ecol Prog Ser 94:43–50

    Article  Google Scholar 

  • Naranjo SA, Carballo JL, García-Gómez JC (1996) Effects of environmental stress on ascidian populations in Algeciras Bay (southern Spain) possible marine bioindicators? Mar Ecol Prog Ser 144:119–131

    Article  Google Scholar 

  • Orton JH (1920) Sea-temperature, breeding and distribution in marine animals. J Mar Biol Assoc UK 12:339–366

    Article  Google Scholar 

  • Osman RW, Whitlatch RB (1998) Local control of recruitment in an epifaunal community and the consequences to colonization processes. Hydrobiologia 375(376):113–123

    Article  Google Scholar 

  • Panagiotou M, Antoniadou C, Krestenitis Y, Chintiroglou C (2007) Stock assessment of the dominant ascidians: Microcosms savignyi, Styela plicata and Phallusia mammillata, in Thessaloniki bay (Thermaikos Gulf). Fresen Environ Bull 16:1012–1019

    CAS  Google Scholar 

  • Panagiotou M, Antoniadou C, Chintiroglou C (2008) Population dynamics and reproductive status of Microcosmus savignyi Monniot, 1962 (Thermaikos Gulf, Eastern Mediterranean): a preliminary assessment. J Nat Hist 42:545–558

    Article  Google Scholar 

  • Pineda MC (2012) A global wanderer: biology, phylogeography and resilience of the introduced ascidian Styela plicata. PhD thesis, Universitat de Barcelona, Barcelona

  • 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:e25495

    Article  CAS  Google Scholar 

  • Pineda MC, López-Legentil S, Turon X (2012) Stress levels over time in the introduced ascidian Styela plicata: the effects of temperature and salinity variations on hsp70 gene expression. Cell Stress Chaperon 17:435–444

    Article  CAS  Google Scholar 

  • Rius M, Pineda MC, Turon X (2009a) Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea. Biol Invasions 11:2181–2194

    Article  Google Scholar 

  • Rius M, Turon X, Marshall DJ (2009b) Non-lethal effects of an invasive species in the marine environment: the importance of early life-history stages. Oecologia 159:873–882

    Article  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 

  • Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu Rev Ecol Syst 31:481–531

    Article  Google Scholar 

  • Sabbadin A (1957) Il ciclo biologico di Ciona intestinalis (L.), Molgula manhattensis (de Kay) e Styela plicata (Lesueur) nella laguna veneta. Arch Oceanog Limnol XI:1–28

  • Sahade R, Tatian M, Esnal GB (2004) Reproductive ecology of the ascidian Cnemidocarpa verrucosa at Potter Cove, South Shetland Islands, Antarctica. Mar Ecol Prog Ser 272:131–140

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Savne I, Lundälv T (1982) Population dynamics and reproductive patterns of Boltenia echinata (Acidiacea) on the Swedish west coast. Neth J Sea Res 16:105–118

    Article  Google Scholar 

  • Sciscioli M, Lepaore E, Tursi A (1978) Relationship between Styela plicata (Les.) (Tunicata) settlement and spawning. Memorie di Biologia Marina e di Oceanografia 8:65–75

    Google Scholar 

  • Shenkar N, Loya Y (2008) The solitary ascidian Herdmania momus: native (Red Sea) versus non-indigenous (Mediterranean) populations. Biol Invasions 10:1431–1439

    Article  Google Scholar 

  • Sims LL (1984) Osmoregulatory capabilities of 3 macrosympatric Stolidobranch ascidians, Styela clava Herdman, Styela plicata (Lesueur), and Styela montereyensis (Dall). J Exp Mar Biol Ecol 82:117–129

    Article  Google Scholar 

  • Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002) Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83:2575–2590

    Article  Google Scholar 

  • Sutherland JP (1974) Multiple stable points in natural communities. Am Nat 108:859–873

    Article  Google Scholar 

  • Svane I, Lundälv T (1981) Reproductive patterns and population dynamics of Ascidia mentula O.F. Müller on the Swedish west coast. J Exp Mar Biol Ecol 50:163–182

    Article  Google Scholar 

  • Svane I, Young C (1989) The biology and behaviour of ascidian larvae. Oceanogr Mar Biol Annu Rev 27:45–90

    Google Scholar 

  • Thiyagarajan V, Qian PY (2003) Effect of temperature, salinity and delayed attachment on development of the solitary ascidian Styela plicata (Lesueur). J Exp Mar Biol Ecol 290:133–146

    Article  Google Scholar 

  • Thornber CS, Kinlan BP, Graham MH, Stachowicz JJ (2004) Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography. Mar Ecol Prog Ser 268:69–80

    Article  Google Scholar 

  • Tucker GH (1942) The histology of the gonads and development of the egg envelopes of an ascidian (Styela plicata Lesueur). J Morphol 70:81–113

    Article  Google Scholar 

  • Turon X (1988) The ascidians of Tossa de Mar (NE Spain). II.-biological cycles of the colonial species. Cah Biol Mar 29:407 − 418

    Google Scholar 

  • 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 342:185–188

    Article  Google Scholar 

  • Tursi A, Matarrese A (1981) Phenomena of settling in Styela plicata (Les.) (Tunicata). Mem Biol Mar Oceanogr 11:117–130

    Google Scholar 

  • Vafidis D, Antoniadou C, Chintiroglou C (2008) Population dynamics, allometric relationships and reproductive status of Microcosmus sabatieri (Tunicata: Ascidiacea) in the Aegean Sea. J Mar Biol Assoc UK 88:1043–1051

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Verween A, Vincx M, Degraer S (2007) The effect of temperature and salinity on the survival of Mytilopsis leucophaeata larvae (Mollusca, Bivalvia): the search for environmental limits. J Exp Mar Biol Ecol 348:111–120

    Article  Google Scholar 

  • Voultsiadou E, Pyrounaki MM, Chintiroglou C (2007) The habitat engineering tunicate Microcosmus sabatieri Roule, 1885 and its associated peracarid epifauna. Estuar Coast Shelf Sci 74:197–204

    Article  Google Scholar 

  • Whitlatch RB, Bullard SG (2007) Introduction to the proceedings of the 1st international invasive sea squirt conference. J Exp Mar Biol Ecol 342:1–2

    Article  Google Scholar 

  • Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666

    Article  Google Scholar 

  • Wong NA, McClary D, Sewell MA (2011) The reproductive ecology of the invasive ascidian, Styela clava, in Auckland Harbour, New Zealand. Mar Biol 158:2775–2785

    Article  Google Scholar 

  • Yamaguchi M (1975) Growth and reproductive cycles of marine fouling Ascidians Ciona intestinalis, Styela plicata, Botrylloides violaceus, and Leptoclinum mitsukurii at Aburatsubo-Moroiso Inlet (Central Japan). Mar Biol 29:253–259

    Article  Google Scholar 

  • Zajac RN, Whitlatch RB, Osman RW (1989) Effects of inter-specific density and food-supply on survivorship and growth of newly settled benthos. Mar Ecol Prog Ser 56:127–132

    Article  Google Scholar 

  • Zerebecki RA, Sorte CJ (2011) Temperature tolerance and stress proteins as mechanisms of invasive species success. PLoS ONE 6:e14806

    Article  CAS  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

We are grateful to E. Arias, C. Torres, A. Pineda, and L. Gelabert for assistance in the field. A. Muntadas and R. Espluga helped in the laboratory. Dr. M. Durfort provided useful comments on the histology. Dr. A. Tursi kindly provided some essential bibliography. Dr. P. Erwin reviewed the manuscript for English grammar. “Ports de la Generalitat” granted collecting permits and access to the harbors. This research was supported by the Marie Curie International Reintegration Grant FP7-PEOPLE-2010-RG 277038 within the 7th European Community Framework Program, by the Spanish Government projects CTM2010-22218 and CTM2010-17755, the Catalan Government grant 2009SGR-484 for Consolidated Research Groups, and by a University of Barcelona APIF fellowship to MCP.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xavier Turon.

Additional information

Communicated by J. P. Grassle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pineda, M.C., López-Legentil, S. & Turon, X. Year-round reproduction in a seasonal sea: biological cycle of the introduced ascidian Styela plicata in the Western Mediterranean. Mar Biol 160, 221–230 (2013). https://doi.org/10.1007/s00227-012-2082-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-012-2082-7

Keywords

Navigation