Marine Biology

, Volume 160, Issue 1, pp 221–230 | Cite as

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

  • M. Carmen Pineda
  • Susanna López-Legentil
  • Xavier Turon
Original Paper

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.

References

  1. Agius BP (2007) Spatial and temporal effects of pre-seeding plates with invasive ascidians: growth, recruitment and community composition. J Exp Mar Biol Ecol 342:30–39CrossRefGoogle Scholar
  2. Allen F (1953) Distribution of marine invertebrates by ships. Aust J Mar Freshw Res 4:307–316CrossRefGoogle Scholar
  3. Altman S, Whitlatch RB (2007) Effects of small-scale disturbance on invasion success in marine communities. J Exp Mar Biol Ecol 342:15–29CrossRefGoogle Scholar
  4. Ballesteros E (1989) Production of seaweeds in Northwestern Mediterranean marine communities: its relation with environmental factors. Sci Mar 53:357–364Google Scholar
  5. Barros R, Rocha R, Pie M (2009) Human-mediated global dispersion of Styela plicata (Tunicata, Ascidiacea). Aquatic Inv 4:45–57CrossRefGoogle Scholar
  6. Becerro MA, Turon X (1992) Reproductive cycles of the ascidians Microcosmus sabatieri and Halocynthia papillosa in the Northwestern Mediterranean. Mar Ecol 13:363–373CrossRefGoogle Scholar
  7. Bingham BL (1997) Light cycles and gametogenesis in three temperate ascidian species. Invertebr Biol 116:61–70CrossRefGoogle Scholar
  8. Blackburn TM, Duncan RP (2001) Determinants of establishment success in introduced birds. Nature 414:195–197CrossRefGoogle Scholar
  9. 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 16:879–891CrossRefGoogle Scholar
  10. 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 342:78–84CrossRefGoogle Scholar
  11. Carlton JT (1989) Mans role in changing the face of the Ocean—biological invasions and implications for conservation of near-shore environments. Conserv Biol 3:265–273CrossRefGoogle Scholar
  12. 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 13–56CrossRefGoogle Scholar
  13. Carlton JT, Geller JB (1993) Ecological roulette—the global transport of nonindigenous marine organisms. Science 261:78–82CrossRefGoogle Scholar
  14. 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 101:8517–8524CrossRefGoogle Scholar
  15. Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110CrossRefGoogle Scholar
  16. Coma R, Ribes M, Gili JM, Zabala M (2000) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453CrossRefGoogle Scholar
  17. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166CrossRefGoogle Scholar
  18. 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
  19. 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
  20. Fine M, Zibrowius H, Loya Y (2001) Oculina patagonica: a non-lessepsian scleractinian coral invading the Mediterranean Sea. Mar Biol 138:1195–1203CrossRefGoogle Scholar
  21. Floerl O, Inglis GJ (2005) Starting the invasion pathway: the interaction between source populations and human transport vectors. Biol Invasions 7:589–606CrossRefGoogle Scholar
  22. 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 13:691–699CrossRefGoogle Scholar
  23. Glasby TM (2001) Development of sessile marine assemblages on fixed versus moving substrata. Mar Ecol Prog Ser 215:37–47CrossRefGoogle Scholar
  24. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27CrossRefGoogle Scholar
  25. 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 78:59–66CrossRefGoogle Scholar
  26. Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion—implications for conservation. Conserv Biol 6:324–337CrossRefGoogle Scholar
  27. 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 120:95–106Google Scholar
  28. Lambert G (2002) Nonindigenous ascidians in tropical waters. Pac Sci 56:291–298CrossRefGoogle Scholar
  29. Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4CrossRefGoogle Scholar
  30. 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
  31. 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
  32. 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 122:179–191CrossRefGoogle Scholar
  33. Mack MC, D’Antonio CM (1998) Impacts of biological invasions on disturbance regimes. Trends Ecol Evol 13:195–198CrossRefGoogle Scholar
  34. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  35. Marchetti MP, Moyle PB, Levine R (2004) Alien fishes in California watersheds: characteristics of successful and failed invaders. Ecol Appl 14:587–596CrossRefGoogle Scholar
  36. Margalef R (1985) Key environments: Western Mediterranean. Pergamon Press, New YorkGoogle Scholar
  37. McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890CrossRefGoogle Scholar
  38. McMahon RF (1996) The physiological ecology of the zebra mussel, Dreissena polymorpha, in North America and Europe. Am Zool 36:339–363Google Scholar
  39. Millar RH (1971) The biology of ascidians. Adv Mar Biol 9:1–100CrossRefGoogle Scholar
  40. Nandakumar K, Tanaka M, Kikuchi T (1993) Interspecific competition among fouling organisms in Tomioka Bay, Japan. Mar Ecol Prog Ser 94:43–50CrossRefGoogle Scholar
  41. 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 144:119–131CrossRefGoogle Scholar
  42. Orton JH (1920) Sea-temperature, breeding and distribution in marine animals. J Mar Biol Assoc UK 12:339–366CrossRefGoogle Scholar
  43. Osman RW, Whitlatch RB (1998) Local control of recruitment in an epifaunal community and the consequences to colonization processes. Hydrobiologia 375(376):113–123CrossRefGoogle Scholar
  44. 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 16:1012–1019Google Scholar
  45. 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 42:545–558CrossRefGoogle Scholar
  46. Pineda MC (2012) A global wanderer: biology, phylogeography and resilience of the introduced ascidian Styela plicata. PhD thesis, Universitat de Barcelona, BarcelonaGoogle Scholar
  47. 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
  48. 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 17:435–444CrossRefGoogle Scholar
  49. Rius M, Pineda MC, Turon X (2009a) Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea. Biol Invasions 11:2181–2194CrossRefGoogle Scholar
  50. 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 159:873–882CrossRefGoogle Scholar
  51. 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 37:621–632Google Scholar
  52. 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 31:481–531CrossRefGoogle Scholar
  53. 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:1–28Google Scholar
  54. 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 272:131–140CrossRefGoogle Scholar
  55. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  56. Savne I, Lundälv T (1982) Population dynamics and reproductive patterns of Boltenia echinata (Acidiacea) on the Swedish west coast. Neth J Sea Res 16:105–118CrossRefGoogle Scholar
  57. Sciscioli M, Lepaore E, Tursi A (1978) Relationship between Styela plicata (Les.) (Tunicata) settlement and spawning. Memorie di Biologia Marina e di Oceanografia 8:65–75Google Scholar
  58. Shenkar N, Loya Y (2008) The solitary ascidian Herdmania momus: native (Red Sea) versus non-indigenous (Mediterranean) populations. Biol Invasions 10:1431–1439CrossRefGoogle Scholar
  59. 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 82:117–129CrossRefGoogle Scholar
  60. 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
  61. Sutherland JP (1974) Multiple stable points in natural communities. Am Nat 108:859–873CrossRefGoogle Scholar
  62. 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 50:163–182CrossRefGoogle Scholar
  63. Svane I, Young C (1989) The biology and behaviour of ascidian larvae. Oceanogr Mar Biol Annu Rev 27:45–90Google Scholar
  64. 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 290:133–146CrossRefGoogle Scholar
  65. 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 268:69–80CrossRefGoogle Scholar
  66. Tucker GH (1942) The histology of the gonads and development of the egg envelopes of an ascidian (Styela plicata Lesueur). J Morphol 70:81–113CrossRefGoogle Scholar
  67. Turon X (1988) The ascidians of Tossa de Mar (NE Spain). II.-biological cycles of the colonial species. Cah Biol Mar 29:407 − 418Google Scholar
  68. 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
  69. Tursi A, Matarrese A (1981) Phenomena of settling in Styela plicata (Les.) (Tunicata). Mem Biol Mar Oceanogr 11:117–130Google Scholar
  70. 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 88:1043–1051CrossRefGoogle Scholar
  71. Vermeij GJ (1996) An agenda for invasion biology. Biol Conserv 78:3–9CrossRefGoogle Scholar
  72. 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 348:111–120CrossRefGoogle Scholar
  73. Voultsiadou E, Pyrounaki MM, Chintiroglou C (2007) The habitat engineering tunicate Microcosmus sabatieri Roule, 1885 and its associated peracarid epifauna. Estuar Coast Shelf Sci 74:197–204CrossRefGoogle Scholar
  74. Whitlatch RB, Bullard SG (2007) Introduction to the proceedings of the 1st international invasive sea squirt conference. J Exp Mar Biol Ecol 342:1–2CrossRefGoogle Scholar
  75. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666CrossRefGoogle Scholar
  76. Wong NA, McClary D, Sewell MA (2011) The reproductive ecology of the invasive ascidian, Styela clava, in Auckland Harbour, New Zealand. Mar Biol 158:2775–2785CrossRefGoogle Scholar
  77. 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 29:253–259CrossRefGoogle Scholar
  78. 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 56:127–132CrossRefGoogle Scholar
  79. Zerebecki RA, Sorte CJ (2011) Temperature tolerance and stress proteins as mechanisms of invasive species success. PLoS ONE 6:e14806CrossRefGoogle Scholar
  80. Zibrowius H (1991) Ongoing modification of the Mediterranean marine fauna and flora by the establishment of exotic species. Mésogée 51:83–107Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • M. Carmen Pineda
    • 1
  • Susanna López-Legentil
    • 1
  • Xavier Turon
    • 2
  1. 1.Department of Animal Biology (Invertebrates)University of BarcelonaBarcelonaSpain
  2. 2.Centre for Advanced Studies of Blanes (CEAB-CSIC)Blanes, GironaSpain

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