Abstract
Over the past decade, several species of non-indigenous ascidians have had adverse effects on a range of coastal ecosystems, and associated industries like aquaculture. One such species, the colonial ascidian Didemnum vexillum, poses a threat to the highly-valued New Zealand green-lipped mussel industry, and there is interest in whether and to what extent its spread can be managed at a regional scale (<100 km). An important component in the decision-making process for managing human-mediated pathways of spread is an understanding of D. vexillum’s natural dispersal potential. Here we use a weight-of-evidence approach, combining laboratory and field studies, to assess the role of natural dispersal mechanisms in the spread of D. vexillum. Under laboratory conditions, >70 % of D. vexillum larvae remained viable and were able to settle and undergo metamorphosis successfully following an artificial delay of 2 h. Larval viability decreased with increasing delay duration, although 10 % of larvae remained viable following a 36 h delay. A field-based study documented larval dispersal from two discrete source populations, with recruitment consistently detected on settlement plates at 250 m from source populations at one experimental site. Exponential decay models used to predict maximum larval dispersal distances at this site indicated that dispersal greater than 250 m is theoretically possible (>1 km in some situations). That being so, we recognise that the successful establishment and persistence of populations will depend on a wide range of processes not taken into account here. Our findings are supported by surveillance of D. vexillum spread in the wider study region; there are a number of instances where the species established on artificial structures that were several kilometres from known source populations, at a time when intensive regional-scale management of anthropogenic vectors was underway. Collectively, our findings indicate that D. vexillum has the ability to spread further by natural dispersal than previously assumed; probably hundreds of metres to kilometres depending on the local hydrological conditions, which has important implications for the ongoing management of this pest species world-wide.
Similar content being viewed by others
References
Adams CM, Shumway SE, Whitlatch RB, Getchis T (2011) Biofouling in marine molluscan shellfish aquaculture: a survey assess the business and economic implications of mitigation. J World Aquacult Soc 42:242–252
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
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 130:51–62
Bennett CE, Marshall DJ (2005) The relative energetic costs of the larval period, larval swimming and metamorphosis for the ascidian Diplosoma listerianum. Mar Freshw Behav Phys 38:21–29
Berrill NJ (1950) The tunicata with an account of the British species. The Ray Society, London
Bingham RL, Young CM (1991) Larval behaviour of the ascidian Ecteinascidia turbinate Herdman: an in situ experimental study of the effects of swimming on dispersal. J Exp Mar Biol Ecol 145:189–204
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
Booth DJ, Brosnan DM (1995) The role of recruitment dynamics in rocky shore and coral reef communities. In: Begon M, Fitter AH (eds) Advances in ecological research. Academic Press, San Diego, pp 309–385
Bullard SG, Sedlack B, Reinhardt JF, Litty C, Gareau K, Whitlatch RB (2007) Fragmentation of colonial ascidians: differences in reattachment capability among species. J Exp Mar Biol Ecol 342:166–168
Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Syst 27:477–500
Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biol Conserv 78:97–106
Castilla JC, Lagos NA, Cerda M (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Mar Ecol Prog Ser 268:119–130
Cie DK, Edwards MS (2011) Vertical distribution of zoospores. Phycologia 50:340–350
Colautti RI, Bailey SA, van Overdijk CDA, Amundsen K, MacIsaac HJ (2006) Characterised and projected costs of nonindigenous species in Canada. Biol Invasion 8:45–59
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 342:154–162
Cowen R, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–446
Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527
Crimaldi J, Thompson J, Rosman J, Lowe R, Koseff J (2002) Hydrodynamics of larval settlement: the influence of turbulent stress events at potential recruitment sites. Limnol Oceanogr 47:1137–1151
Davis AR, Butler AJ (1989) Direct observations of larval dispersal in the colonial ascidian Podoclavella moluccensis Sluiter: evidence for closed populations. J Exp Mar Biol Ecol 127:189–203
Degnan BM, Johnson CR (1999) Inhibition of settlement and metamorphosis of the ascidian Herdmania curvata by non-geniculate coralline algae. Biol Bull 197:332–340
Fiksen O, Jørgensen C, Kristiansen T, Vikebø F, Huse G (2007) Linking behavioural ecology and oceanography: larval behaviour determines growth, mortality and dispersal. Mar Ecol Prog Ser 347:195–205
Fletcher LM, Forrest BM (2011) Induced spawning and culture techniques for the invasive ascidian Didemnum vexillum (Kott, 2002). Aquat Invasion 6:457–464
Fletcher LM, Bell JJ, Forrest BM (2009) Reproductive seasonality of the invasive ascidian Didemnum vexillum: management options for mitigating impacts on the New Zealand Greenshell™ mussel industry. Sixth international conference on marine bioinvasions: marine bioinvaders, agents of change in a changing world. Portland, OR, USA, 24–27 Aug 2009
Floerl O, Inglis GJ (2005) Starting the invasion pathway: the interaction between source populations and human transport vectors. Biol Invasion 7:589–606
Forrest BM, Brown SN, Taylor MD, Hurd CL, Hay CH (2000) The role of natural dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales, Phaeophyceae). Phycologia 39:547–553
Forrest BM, Gardener JPA, Taylor MD (2009) Internal borders for managing invasive marine species. J Appl Ecol 46:46–54
Gaines SD, Gaylord B, Gerber LR, Hastings A, Kinlan BP (2007) Connecting places: the ecological consequences of dispersal in the sea. Oceanography 20:90–99
Gosselin LA, Qian P-Y (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282
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
Hopkins GA, Forrest BM, Piola RF, Gardner JPA (2010) Factors affecting survivorship of defouled communities and the effect of fragmentation on establishment success. J Exp Mar Biol Ecol 396:233–243
Huret M, Petitgas P, Woillez M (2010) Dispersal kernels and their drivers captured with a hydrodynamic model and spatial indices: a case study on anchovy (Engraulis encrasicolus) early life stages in the Bay of Biscay. Prog Oceanogr 87:6–17
Jaeckle WB (1994) Rates of energy consumption and acquisition by lecithotrophic larvae of Bugula neritina (Bryozoa: Cheliostomata). Mar Biol 119:517–523
Jaeckle WB, Manahan DT (1989) Feeding by “nonfeeding larva”: uptake of dissolved amino acids from seawater by lecithotrophic larvae of the gastropod Haliotis rufescens. Mar Biol 103:87–89
Johnston EL, Piola RF, Clark G (2009) The role of propagule pressure in invasion success. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems: ecological, management, and geographic perspectives. Springer, Berlin, pp 133–151
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241
Keough MJ, Downes BJ (1982) Recruitment of marine invertebrates: the role of active larval choices and early mortality. Oecologia 54:348–352
Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020
Kinlan BP, Gaines SD, Lester SE (2005) Propagule dispersal and the scales of marine community process. Divers Distrib 11:139–148
Knights AM, Crowe TP, Burnell G (2006) Mechanisms of larval transport: vertical distribution of bivalve larvae varies with tidal conditions. Mar Ecol Prog Ser 326:167–174
Kott P (2002) A complex didemnid ascidian from Whangamata, New Zealand. J Mar Biol Assoc UK 82:625–628
Lambert G (2002) Nonindigenous ascidians in tropical waters. Pac Sci 56:291–298
Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342:3–4
Lambert G (2009) Adventures of a sea squirt sleuth: unravelling the identity of Didemnum vexillum, a global ascidian invader. Aquat Invasion 4:5–28
Lengyel NL, Collie JS, Valentine PC (2009) The invasive colonial ascidian Didemnum vexillum on Georges Bank—ecological effects and genetic identification. Aquat Invasion 4:143–152
Leung B, Mandrak NE (2007) The risk of establishment of aquatic invasive species: joining invasibility and propagule pressure. Proc R Soc B Biol Sci 274:2603–2609
Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integr Comp Biol 46:282–297
Lockwood JL, Cassey P, Blackburn TM (2009) The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Divers Distrib 15:904–910
Manriquez PH, Castilla JC (2007) Roles of larval behaviour and microhabitat traits in determining spatial aggregations in the ascidian Pyura chilensis. Mar Ecol Prog Ser 332:155–165
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, Strother JA (2003) The kinematics of phototaxis in larvae of the ascidian Aplidium constellatum. Mar Biol 142:173–184
McQuaid CD, Phillips TE (2000) Limited wind-driven dispersal of intertidal mussel larvae: in situ evidence from the plankton and the spread of the invasive species Mytilus galloprovincialis in South Africa. Mar Ecol Prog Ser 201:211–220
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492
Morgan SG (1995) Life and death in the plankton: larval mortality and adaptation. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 279–322
Morris JA Jr, Carman MR (2012) Fragment reattachment, reproductive status, and health indicators of the invasive colonial tunicate Didemnum vexillum with implications for dispersal. Biol Invasion. doi:10.1007/s10530-012-0219-8
Myers JH, Simberloff D, Kuris AM, Carey JR (2000) Eradication revisited: dealing with exotic species. Trends Ecol Evol 15:316–320
Norkko A, Cummings VJ, Thrush SF, Hewitt JE, Hume T (2001) Local dispersal of juvenile bivalves: implications for sandflat ecology. Mar Ecol Prog Ser 212:131–144
Olson RR (1985) The consequences of short-distance larval dispersal in a sessile marine invertebrate. Ecology 66:30–39
Olson RR, McPherson R (1987) Potential vs. realized larval dispersal: fish predation on larvae of the ascidian Lissoclinum patella (Gottschaldt). J Exp Mar Biol Ecol 110:245–256
Osman RW, Whitlatch RB (2004) The control of the development of a marine benthic community by predation on recruits. J Exp Mar Biol Ecol 311:117–145
Palumbi SR (2003) Population genetics, demographic connectivity and the design of marine protected areas. Ecol Appl 13:S146–S158
Pechenik SR (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297
Pechenik JA, Rittschof D, Schmidt AR (1993) Influence of delayed metamorphosis on survival and growth of juvenile barnacles Balanus Amphitrite. Mar Biol 115:287–294
Pechenik JA, Wendt DE, Jarrett JN (1998) Metamorphosis is not a new beginning. Bioscience 48:901–910
Petersen JK, Svane I (1995) Larval dispersal in the ascidian Ciona intestinalis (L.). Evidence for a closed population. J Exp Mar Biol Ecol 186:89–102
Pimental D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 59:53–65
Pineda J, Hare JA, Sponaugle S (2007) Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography 20:22–39
Puth LM, Post DM (2005) Studying invasion: have we missed the boat? Ecol Lett 8:715–721
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN:3-900051-07-0; http://www.R-project.org/
Ramsay A, Davidson J, Landry T, Arsenault G (2008) Process of invasiveness among exotic tunicates in Prince Edward Island, Canada. Biol Invasion 10:1311–1316
Rilov G, Crooks JA (2008) Marine bioinvasions: conservation hazards and vehicles for ecological understanding. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems: ecological, management, and geographic perspectives. Springer, Berlin, pp 3–12
Rius M, Branch GM, Griffiths CL, Turon X (2010) Larval settlement behaviour in six gregarious ascidians in relation to adult distribution. Mar Ecol Prog Ser 418:151–163
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
Rumrill SS (1990) Natural mortality of marine invertebrate larvae. Ophelia 32:163–198
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
Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385
Shanks AL, Shearman RK (2009) Paradigm lost? Cross-distributions of intertidal invertebrate larvae were unaffected by upwelling or downwelling. Mar Ecol Prog Ser 385:189–204
Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:S159–S169
Sombardier L, Niiler PP (1994) Global surface circulation measured by Lagrangian drifters. Sea Technol 35:21–24
StatSoft Inc. (2008) STATISTICA (data analysis software system), version 8.0. www.statsoft.com
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 Invasion 4:29–44
Stoner DS (1990) Recruitment of a tropical colonial ascidian: relative importance of pre-settlement vs. post-settlement processes. Ecology 71:1682–1690
Strathmann RR, Hughes TP, Kuris AM, Lindeman KC, Morgan SG, Pandolfi JM, Warner RR (2002) Evolution of local recruitment and its consequences for marine populations. Bull Mar Sci 70:377–396
Svane I, Dolmer P (1995) Perception of light at settlement: a comparative study of two invertebrate larvae, a scyphozoan planula and a simple ascidian tadpole. J Exp Mar Biol Ecol 187:51–61
Svane I, Young CM (1989) The ecology and behaviour of ascidian larvae. Oceanogr Mar Biol 27:45–90
Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45
Valentine PC, Collie JS, Reid RN, Asch RG, Guida VG, Blackwood DS (2007) The occurrence of the colonial ascidian Didemnum sp. on Georges Bank gravel habitat: ecological observations and potential effects on groundfish and scallop fisheries. J Exp Mar Biol Ecol 342:179–181
Valentine PC, Carman MR, Dijkstra J, Blackwood DS (2009) Larval recruitment of the invasive colonial ascidian Didemnum vexillum, seasonal water temperatures in New England coastal and offshore waters, and implications for spread of the species. Aquat Invasion 4:153–168
Verling E, Ruiz GM, Smith LD, Galil B, Miller AW, Murphy KR (2005) Supply-side invasion ecology: characterizing propagule pressure in coastal ecosystems. Proc R Soc B Biol Sci 272:1249–1257
Weidner RT, Sells RL (1973) Elementary modern physics, 2nd edn. Allyn & Bacon, Inc., Boston
Wendt DE, Johnson CH (2006) Using latent effects to determine the ecological importance of dissolved organic matter to marine invertebrates. Integr Comp Biol 46:634–642
Woollacott RM, Pechenik JA, Imbalzano KM (1989) Effects of duration of larval swimming period on early colony development in Bugula stolonifera (Bryozoa: Cheilostomata). Mar Biol 102:57–63
Worcester SE (1994) Adult rafting versus larval swimming: dispersal and recruitment of a bottrylid ascidian on eelgrass. Mar Biol 121:309–317
Young CM (1986) Direct observations of field swimming behaviour in larvae of the colonial ascidian Ecteinascidia turbinate. Bull Mar Sci 39:279–289
Young CM, Braithwaite LF (1980) Larval behavior and post-settling morphology in the ascidian, Chelyosoma productum Stimpson. J Exp Mar Biol Ecol 42:157–169
Acknowledgments
We are grateful to Richard Piola, Grant Hopkins, Kirsty Smith, Weimin Jiang (Cawthron Institute) and James Brodie for their assistance with various aspects of the experiments and data analysis, as well as an anonymous reviewer whose helpful comments improved this manuscript. Sincere thanks is also expressed to New Zealand King Salmon Ltd, in particular staff at the Ruakaka Bay farm, who provided considerable logistic support for this project, as well as Aaron Pannell of Marlborough Mussels Ltd for access to the results of the monitoring program and valuable insight into the spread of this species. This work was funded by the New Zealand Ministry of Science and Innovation as part of Contract C01X0502 (Effective Management of Marine Biodiversity and Biosecurity). L. Fletcher was funded through a joint Cawthron Institute and New Zealand Tertiary Education Commission ‘Bright Futures Enterprise PhD Scholarship’.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fletcher, L.M., Forrest, B.M. & Bell, J.J. Natural dispersal mechanisms and dispersal potential of the invasive ascidian Didemnum vexillum . Biol Invasions 15, 627–643 (2013). https://doi.org/10.1007/s10530-012-0314-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-012-0314-x