Abstract
Exotic species invasions are one of the greatest threats to marine systems and ascidians have many characteristics that favor transport, colonization and establishment into new regions. Didemnum perlucidum is a widespread species that has been introduced into tropical ports around the world. Here we examine the colonizing ability of D. perlucidum by experimental use of artificial plates in a shellfish culture. The experiment comprised paired plates for colonization (bare and occupied) in 16 monthly replicates. Recruitment and space occupation were compared between bare and occupied plates and an estimation of reproductive effort was based on the number of larvae produced in each of ten colonies collected on the culture structures. D. perlucidum reproduced continuously but greatest reproduction occurred between December 2006 and May 2007. While recruitment was somewhat greater (number of new colonies) on bare plates, this species can colonize already occupied substrates and, surprisingly, colony area was always similar between treatments. Thus, while fewer colonies formed on occupied plates, once formed, colonies grew at rates similar to those on clean plates. Thus, D. perlucidum colonizes substrates very efficiently, especially when unoccupied space is available.
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Altman S, Whitlatch RB (2007) Effects of small-scale disturbance on invasion success in marine communities. J Exp Mar Biol Ecol 342:15–29
Becerro MA, Turon X (1992) Reproductive cycles of the ascidians Microcosmus sabatieri wand Halocynthia papillosa in the northwestern Mediterranean. Mar Ecol 13:363–373
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 342:5–14
Britton-Simmons KH (2006) Functional group diversity, resource preemption and the genesis of invasion resistance in a community of marine algae. Oikos 113:395–401
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 (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
Bulleri F, Airoldi L, Branca GM, Abbiati M (2006) Positive effects of the introduced green alga, Codium fragile ssp tomentosoides, on recruitment and survival of mussels. Mar Biol 148:1213–1220
Buss LW (1986) Competition and community organization on hard surfaces in the sea. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, New York, pp 517–536
Buss LW, Jackson JBC (1979) Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am Nat 113(2):223–234
Carlton JT, Geller JB (1993) Ecological roulette: biological invasion and the global transport of nonindigenous marine organisms. Science 261:78–82
Carman MR, Bullard SG, Donnelly JP (2007) Water quality, nitrogen pollution, and ascidian diversity in coastal waters of southern Massachussetts, USA. J Exp Mar Biol Ecol 342:175–178
Carver CE, Chisholm A, Mallet AL (2003) Strategies to mitigate the impact of Ciona intestinalis (l) biofouling on shellfish production. J Shellfish Res 22(3):621–631
Castilla J, Guiñez R, Caro AU, Ortiz V (2004a) Invasion of a rocky intertidal shore by the tunicate Pyura praeputialis in the Bay of Antofagasta, Chile. Proc Natl Acad Sci USA 101(23):8517–8524
Castilla JC, Lagos NA, Cerda M (2004b) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Mar Ecol Prog Ser 268:119–130
Chapman JW, Carlton JT (1991) A test of criteria for introduced species: the global invasion by the isopod Synidotea laevidorsalis (Miers, 1881). J Crustacean Biol 11(3):386–400
Colautti RI, Grigorovich IA, MacIsaac HJ (2006) Propagule pressure: a null model for biological invasions. Biol Invasions 8(5):1387–3547
Coutts ADM, Dodgshun TJ (2007) The nature and extent of organisms in vessel sea-chests: a protected mechanism for marine bioinvasions. Mar Pollut Bull 54:875–886
Davis AR (1991) Alkaloids and ascidian chemical defense: evidence for the ecological role of natural products from Eudistoma olivaceum. Mar Biol 111:375–379
Davis AR (1996) Association among ascidians: facilitation of recruitment in Pyura spinifera. Mar Biol 126:35–41
Davis MH, Davis ME (2007) The distribution of Styela clava (Tunicata, Ascidiacea) in European waters. J Exp Mar Biol Ecol 342:182–184
Dias GM, Delboni CGM, Duarte LFL (2008) Effects of competition on sexual and clonal reproduction of a tunicate: the importance of competitor identity. Mar Ecol Prog Ser 362:149–156
Dustan PK, Johnson CR (2002) Invasion rates increase with species richness in a marine epibenthic community by two mechanisms. Oecologia 138:285–292
Elkin C, Marshall DJ (2007) Desperate larvae: influence of deferred costs and habitat requirements on habitat selection. Mar Ecol Prog Ser 335:143–153
Getchis TS (2006) What’s putting some aquaculturists in a “foul” mood. http://digitalcommonsuconnedu/wracklines/18. Cited 1 Nov 2007
Gittenberger A (2007) Recent population expansions of non-native ascidians in the Netherlands. J Exp Mar Biol Ecol 342:122–126
Global Ballast Water Management Programme (2008) International Marine Organization. http://globallastimoorg. Cited 27 Feb 2008
Golbuu Y, Bauman A, Kuartei J, Victor S (2005) The state of coral reef ecosystem of Palau. In: Waddell J (ed) The state of coral reef ecosystems of the United States and Pacific freely associated states. NOAA Technical Memorandum NOS NCCOS 11, NOAA/NCCOS Center for Coastal Monitoring and Assessment’s Biogeography. Team Silver Spring, Maryland, pp 488–507
Gottelli NJ (1987) Spatial and temporal patterns of reproduction, larval settlement, and recruitment of the compound ascidian Aplidium stellatum. Mar Biol 94(1):45–51
Green KM, Russell BD, Clark RJ, Jones MK, Garson MJ, Skilleter GA, Degnan BM (2002) A sponge allelochemical induces ascidian settlement but inhibits metamorphosis. Mar Biol 140:355–363
Grosberg RK (1981) Competitive ability influences habitat choice in marine invertebrates. Nature 290:700–702
Hirose E, Kojima A, Nogami J, Teruya K (2007) Seasonality of sexual reproduction in three photosymbiotic Trididemnum species (Didemnidae: Ascidiacea: Tunicata) in a subtropical sea grass bed. J Mar Biol Assoc UK 87:979–982
Hurlbut CJ (1993) The adaptive value of larval behavior of a colonial ascidian. Mar Biol 115(2):253–262
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16(4):199–204
Krug PJ (2006) Defense of benthic invertebrates against surface colonization by larvae: a chemical arms race. Progress in molecular and subcellular biology subseries marine molecular biotechnology. In Fusetani N, Clare AS (eds) Antifouling compounds. Springer-Verlag, Berlin
Lambert G (2002) Nonindigenous ascidians in tropical waters. Pac Sci 56(3):291–298
Lambert G (2003) Marine biodiversity of Guam: the Ascidiacea. Micronesica 35–36:588–597
Lambert G (2005) Ecology and natural history of the protochordates. Can J Zool 83:34–50
Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4
Lambert CC, Lambert G (1998) Non-indigenous ascidians in southern California harbors and marinas. Mar Biol 130:675–688
Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbours of the Southern California Bight. Mar Ecol Prog Ser 259:145–161
LeBlanc N, Davidson J, Tremblay R, McNiven M, Landry T (2007) The effect of anti-fouling treatments for the clubbed tunicate on the blue mussel, Mytilus edulis. Aquaculture 264:205–213
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20(5):223–228
Marenzi AWC, Gesner AF, Almeida TCM, Corbeta R (2006) Comunidade macrobentônica da Armação do Itapocoroy Penha SC. In: Branco JO, Marenzi AWC (eds) Bases ecológicas para um desenvolvimento sustentável: estudos de caso em Penha, SC. Editora Univali, Itajaí, pp 133–152
Marshall DJ, Pechenik JA, Keough MJ (2003) Larval activity levels and delayed metamorphosis affect post-larval performance in the colonial ascidian Diplosoma listerianum. Mar Ecol Prog Ser 246:153–162
McHenry MJ (2005) The morphology, behavior, and biomechanics of swimming in ascidian larvae. Can J Zool 83:62–74
Monniot F (1983) Ascidies littorales de Guadeloupe I Didemnidae. Bull Mus Hist Nat 4ª ser 5 A(1):5–49
Monniot C, Monniot F (1997) Ascidians collected in Tanzania. J East Afr Nat Hist 86:1–35
Nandakumar K (1996) Importance of timing of panel exposure on the competitive outcome and succession of sessile organisms. Mar Ecol Prog Ser 131(1–3):191–203
Oren U, Benayahu Y (1998) Didemnid ascidians: rapid colonizers of artificial reefs in Eilat (Red Sea). Bull Mar Sci 63(1):199–206
Osman RW, Whitlatch RB (1995a) The influence of resident adults on larval settlement: experiments with four species of ascidians. J Exp Mar Biol Ecol 190:199–220
Osman RW, Whitlatch RB (1995b) The influence of resident adults on recruitment: a comparison to settlement. J Exp Mar Biol Ecol 190:169–198
Osman RW, Whitlatch RB (1998) Local control of recruitment in an epifaunal community and the consequences to colonization processes. Hydrobiology 375–376:113–123
Osman RW, Whitlatch RB (2007) Variation in the ability of Didemnum sp to invade established communities. J Exp Mar Biol Ecol 342:40–53
Rocha RM (1991) Replacement of the compound ascidian species in a southeastern Brazilian fouling community. Bolm Inst Oceonogr 39(2):141–153
Rocha RM, Faria SB (2005) Ascidians at Currais islands, Paraná, Brazil: taxonomy and distribution. Biota Neotrop 5(2):1–20
Rocha RM, Kremer LP (2005) Introduced Ascidians in Paranaguá Bay, Paraná, southern Brazil. Rev Bras Zool 22(4):1170–1184
Rocha RM, Monniot F (1995) Taxonomic and ecological notes on some Didemnum species (Ascidiacea, Didemnidae) from São Sebastião Channel, South-Eastern Brazil. Rev Bras Biol 55(4):639–649
Rocha RM, Nasser CM (1998) Some ascidians (Tunicata, Ascidiacea) from Paraná State, Southern Brazil. Rev Bras Zool 15:633–642
Rocha RM, Moreno TR, Metri R (2005) Ascídias (Tunicata, Ascidiacea) da Reserva Biológica Marinha do Arvoredo, Santa Catarina, Brasil. Rev Bras Zool 22(2):461–476
Rocha RM, Kremer LP, Baptista MS, Metri R (2009) Bivalve cultures provide habitat for exotic tunicates in southern Brazil. Aquat Invasions 4(1):195–205
Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8(4):927–939
Ruiz GM, Fofonoff P, 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
Schettini CAF, Carvalho JLB, Truccolo EC (1999) Aspectos hidrodinâmicos da Enseada da Armação de Itapocoroy, SC. Notas Tec Facimar 3:99–109
Souza RCCL, Fernandes FC, Silva EP (2004) Distribuição atual do mexilhão Perna perna no mundo: um caso recente de bioinvasão. In: Silva JSV, Souza RCCL (eds) Água de lastro e bioinvasão. Interciência, Rio de Janeiro, pp 157–172
Stachowicz JJ, Byrnes JE (2006) Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors. Mar Ecol Prog Ser 311:251–262
Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579
Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002a) Biodiversity, invasion resistance and marine ecosystem function: reconciling patterns and process. Ecology 83(9):2575–2590
Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002b) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci USA 6:15497–15500
Sutherland JP (1974) Multiple stable points in natural communities. Am Nat 108(964):859–873
Svane IB, Young CM (1989) The ecology and behaviour of ascidian larvae. Oceanogr Mar Biol Annu Rev 27:45–90
Thieltges DW, Strasser M, Van Beusekom JEE, Reise K (2004) Too cold to prosper—winter mortality prevents population increase of the introduced American slipper limpet Crepidula fornicata in northern Europe. J Exp Mar Biol Ecol 311:375–391
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
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 342:109–121
Young CM, Chia F (1981) Laboratory evidence for delay of larval settlement in response to a dominant competitor. Int J Invertebr Reprod 3:221–226
Acknowledgments
We thank M. Baptista, J. Beneti, N. Bonnet, E. Bornancin, L. Cangussu, H. Heyse, F. Menon, and T. Zanata for field assistance. A. Marenzi, G. Manzoni and UNIVALI for the logistics in Penha. We also thank CNPq for the scholarship to LPK and for the research grant to RMR. This is the contribution 1751 of the Zoology Department, Universidade Federal do Paraná (UFPR).
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Kremer, L.P., Rocha, R.M. & Roper, J.J. An experimental test of colonization ability in the potentially invasive Didemnum perlucidum (Tunicata, Ascidiacea). Biol Invasions 12, 1581–1590 (2010). https://doi.org/10.1007/s10530-009-9571-8
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DOI: https://doi.org/10.1007/s10530-009-9571-8