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Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea

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Abstract

Marine introductions are a serious threat for biodiversity, especially in seas where shipping is intensive. Microcosmus squamiger is a widespread marine invader that can alter native biota and it is therefore imperative to understand its biology and ecology. We studied the population dynamics and reproductive cycles of M. squamiger over a 2-year period, as well as its settlement and colonization patterns, in a north-western Mediterranean (NE Spain) locality where M. squamiger has been introduced. All biological parameters showed a strong seasonal pattern that peaked in summer with a major spawning episode at the end of summer. Size-frequency histograms indicated a 2-year cycle. Colonization experiments suggested that M. squamiger recruitment mortality is high and requires a well structured community. In addition, we monitored the abundance of the native predator Thais haemastoma, which showed a significant positive correlation with M. squamiger biomass, indicating its potential usefulness as a biological control.

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References

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

    Article  Google Scholar 

  • Bingham BL (1997) Light cycles and gametogenesis in three temperate ascidian species. Inverteb Biol 116:61–70. doi:10.2307/3226925

    Article  Google Scholar 

  • Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44:32–38. doi:10.1016/S0025-326X(01)00150-3

    Article  CAS  PubMed  Google Scholar 

  • Bullard SG, Lambert G, Carman MR, Byrnes J, Whitlatch RB, Ruiz G et al (2007) The colonial ascidian Didemnum sp A: Current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America. J Exp Mar Biol Ecol 342:99–108. doi:10.1016/j.jembe.2006.10.020

    Article  Google Scholar 

  • Castilla JC, Guiñez 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. doi:10.1073/pnas.0401921101

    Article  CAS  PubMed  Google Scholar 

  • Coma R, Ribes M (2003) Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101:205–215. doi:10.1034/j.1600-0706.2003.12028.x

    Article  Google Scholar 

  • Coma R, Ribes M, Gili J-M, Zabala M (2000) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453. doi:10.1016/S0169-5347(00)01970-4

    Article  PubMed  Google Scholar 

  • da Rocha RM, da Cruz Lotufo TM, de Almeida Rodrigues S (1999) The biology of Phallusia nigra Savigny, 1816 (Tunicata: Ascidiacea) in southern Brazil: spatial distribution and reproductive cycle. Bull Mar Sci 64:77–87

    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. doi:10.3354/meps244125

    Article  Google Scholar 

  • deRivera CE, Hitchcock NG, Teck SJ, Steves BP, Hines AH, Ruiz GM (2007) Larval development rate predicts range expansion of an introduced crab. Mar Biol 150:1275–1288

    Article  Google Scholar 

  • Eckman JE (1996) Closing the larval loop: linking larval ecology to the population dynamics of marine benthic invertebrates. J Exp Mar Biol Ecol 200:207–237

    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 

  • Galil BS (2000) A sea under siege—alien species in the Mediterranean. Biol Invasions 2:177–186

    Article  Google Scholar 

  • Galil BS (2007) Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar Poll Bull 55:314–322

    Article  CAS  Google Scholar 

  • Giangrande A, Geraci S, Belmonte G (1994) Life cycle and life history diversity in marine invertebrates and the implications in community dynamics. Ocean Mar Biol 32:305–333

    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 Cons 78:59–66

    Article  Google Scholar 

  • Kott P (1985) The Australian Ascidiacea, Part 1. Phlebobranchia and Stolidobranchia. Mem Queensland Mus 23:1–438

    Google Scholar 

  • Kyle R, Pearson B, Fielding PJ, Robertson WD, Birnie SL (1997) Subsistence shellfish harvesting in the Maputaland marine reserve in northern Kwazulu-Natal, South Africa: rocky shore organisms. Biol Cons 82:183–192

    Article  Google Scholar 

  • Lafferty KD, Kuris AM (1996) Biological control of marine pests. Ecology 77:1989–2000

    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 

  • 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 

  • Lowe AJ (2002) Microcosmus squamiger; a solitary ascidian introduced to southern California harbors and marinas: salinity tolerance and phylogenetic analysis. MSc Thesis. California State University, Fullerton

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Marshall DJ (2002) In situ measures of spawning synchrony and fertilization success in an intertidal, free-spawning invertebrate. Mar Ecol Prog Ser 236:113–119

    Article  Google Scholar 

  • Mastrototaro F, Dappiano M (2005) New record of the non-indigenous species Microcosmus squamiger (Ascidiacea: Stolidobranchia) in the harbour of Salerno (Tyrrhenian Sea, Italy). J Mar Biol Assoc UK 85:1555

    Article  Google Scholar 

  • Michaelsen VW (1927) Einige neue westaustralische Ptychobranchiate Ascidien. Zool Anz 71:193–203

    Google Scholar 

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

    Article  Google Scholar 

  • Monniot C (1962) Les Microcosmus des cotes de France. Vie Milieu 12:397–432

    Google Scholar 

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

    Google Scholar 

  • Monniot C (2002) Stolidobranch ascidians from the tropical western Indian Ocean. Zool J Linn Soc 135:65–120

    Article  Google Scholar 

  • Monniot C, Monniot F, Griffiths CL, Schleyer M (2001) South African Ascidians. Ann S Afr Mus 108:1–141

    Google Scholar 

  • Monteiro SM, Chapman MG, Underwood AJ (2002) Patches of the ascidian Pyura stolonifera (Heller, 1878): structure of habitat and associated intertidal assemblages. J Exp Mar Biol Ecol 270:171–189

    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 

  • Naranjo SA, García-Gómez JC (1994) Ascidias litorales del estrecho de Gibraltar: nuevas aportaciones faunísticas. Graellsia 50:57–69

    Google Scholar 

  • Noonburg EG, Byers JE (2005) More harm than good: when invader vulnerability to predators enhances impact on native species. Ecology 86:2555–2560

    Article  Google Scholar 

  • Occhipinti Ambrogi A (2000) Biotic invasions in a Mediterranean Lagoon. Biol Invasions 2:165–176

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Papaconstantinou C (1990) The spreading of lessepsian fish migrants into the Aegean Sea (Greece). Sci Mar 54:313–316

    Google Scholar 

  • Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, Von Holle B, Moyle PB, Byers JE, Goldwasser L (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19

    Article  Google Scholar 

  • Pérez-Portela R, Palacín C, Duran S, Turon X (2007) Biological traits of three closely related species of Pycnoclavella (Ascidiacea) in the Western Mediterranean. Mar Biol 152:1031–1038

    Article  Google Scholar 

  • Piazzi L, Ceccherelli G, Cinelli F (2001) Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar Ecol Prog Ser 210:149–159

    Article  Google Scholar 

  • Primo C, Vázquez E (2004) Zoogeography of the southern African ascidian fauna. J Biogeogr 31:1987–2009

    Article  Google Scholar 

  • Ranasinghe JA, Mikel TK, Velarde RG, Weisberg SB, Montagne DE, Cadien DB, Dalkey A (2005) The prevalence of non-indigenous species in southern California embayments and their effects on benthic macroinvertebrate communities. Biol Invasions 7:679–686

    Article  Google Scholar 

  • Rilov G, Gasith A, Benayahu Y (2002) Effect of an exotic prey on the feeding pattern of a predatory snail. Mar Env Res 54:85–98

    Article  CAS  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 colonisations. Divers Distrib 14:818–828

    Article  Google Scholar 

  • Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939

    Article  Google Scholar 

  • 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 27:337–343

    Article  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. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Shenkar N, Loya Y (2008) The solitary ascidian Herdmania momus: native (Red Sea) versus non-indigenous (Mediterranean) populations. Biol Invasions. doi:10.1007/s10530-008-9217-2

  • 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 

  • Streftaris N, Zenetos A (2006) Alien marine species in the mediterranean—the 100 ‘Worst Invasives’ and their impact. Medit Mar Sci 7:87–118

    Google Scholar 

  • Svane I (1983) Ascidian reproductive patterns related to long-term population dynamics. Sarsia 68:249–255

    Google Scholar 

  • Svane I, Lundalv T (1982) Persistence stability in ascidian populations: long-term population dynamics and reproductive pattern of Pyuna tessellata (Forbes) in Gullmarfjorden on the Swedish west coast. Sarsia 67:249–257

    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 

  • Turon X, Becerro MA (1992) Growth and survival of several ascidian species from the northwestern mediterranean. Mar Ecol Prog Ser 82:235–247

    Article  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 

  • Wasson K, Zabin CJ, Bedinger L, Diaz MC, Pearse JS (2001) Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biol Cons 102:143–153

    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 

  • 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 29:253–259

    Article  Google Scholar 

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

    Google Scholar 

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Acknowledgements

We are grateful to A. Bucci and I. Calderón for assistance in the field. We thank P.A. Maíllo and M. Durfort for their help with the histological procedures. This study was funded by project CTM2007-66635 of the Spanish Government.

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Correspondence to Xavier Turon.

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Rius, M., Pineda, M.C. & Turon, X. Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea. Biol Invasions 11, 2181–2194 (2009). https://doi.org/10.1007/s10530-008-9375-2

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