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Adapted for invasion? Comparing attachment, drag and dislodgment of native and nonindigenous hull fouling species

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Abstract

Invasive species possess unique traits that allow them to navigate the invasion process in order to establish and spread in new habitats. Successful hull fouling invaders must resist both physical and physiological stressors associated with their voyage. We characterised attachment strength and drag coefficient of common fouling species in order to estimate the velocity required to dislodge them from boat hulls. We hypothesized nonindigenous fouling species would possess biomechanical properties that enable them to remain attached to hulls more successfully than similar native species. Indeed, the well-known invasive ascidian Styela clava had both high attachment strength and low drag coefficient and its dislodgment velocity was well above that of fast moving vessels. In contrast, the native congener Styela gibbsii had low attachment strength and higher drag coefficient. Colonial invasive species employed a different hitchhiking strategy; despite their low attachment strengths, Botrylloides violaceus and Didemnum vexillum had low drag coefficients allowing them to be transported on slower-moving vessels, such as sailboats and barges. The biomechanical adaptations of invasive species show promise in predicting future invaders and informing vector management strategies at the first node in the invasion process: transport by the vector.

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References

  • Abbott DP, Johnson JV (1972) The ascidians Styela barnharti, S. plicata, S. clava, and S. montereyensis in Californian waters. Bull South Calif Acad Sci 71:95–105

    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 

  • Anderson K, Close L, DeWreede RE, Lynch BJ, Ormond C, Walker M (2006) Biomechanical properties and holdfast morphology of coenocytic algae (Halimedales, Chlorophyta) in Bocas del Toro, Panama. J Exp Mar Biol Ecol 328:155–167

    Article  Google Scholar 

  • Bell EC (1999) Applying flow tank measurements to the surf zone: predicting dislodgment of the Gigartinaceae. Phycol Res 47:159–166

    Article  Google Scholar 

  • Bell CM, Gosline JM (1996) Mechanical design of mussel byssus: material yield enhances attachment strength. J Exp Biol 199:1005–1017

    PubMed  Google Scholar 

  • Bell EC, Gosline JM (1997) Strategies for life in flow: tenacity, morphometry, and probability of dislodgment of two Mytilus species. Mar Ecol Prog Ser 159:197–208

    Article  Google Scholar 

  • Boller ML, Carrington E (2006) The hydrodynamic effects of shape and size change during reconfiguration of a flexible macroalga. J Exp Biol 209:1894–1903

    Article  PubMed  Google Scholar 

  • Bossenbroek JM, Johnson LE, Peters B, Lodge DM (2007) Forecasting the expansion of zebra mussels in the United States. Cons Bio 21:800–810

    Article  Google Scholar 

  • Byers JEB (2002) Impact of non-indigenous species on natives enhanced by anthropogenic alteration of selection regimes. Oikos 97:449–458

    Article  Google Scholar 

  • Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biol Conserv 78:97–106

    Article  Google Scholar 

  • Carrington E (1990) Drag and dislodgement of an intertidal macroalga: consequences of morphological variation in Mastocarpus papillatus Kutzing. J Exp Mar Biol Ecol 139:185–200

    Article  Google Scholar 

  • Carrington E (2002) Seasonal variation in the attachment strength of blue mussels: causes and consequences. Limnol Oceanog 47:1723–1733

    Article  Google Scholar 

  • Clarke Murray C, Pakhomov EA, Therriault TW (2011) Recreational boating: a large unregulated vector transporting marine invasive species. Divers Distrib 17:1161–1172

    Article  Google Scholar 

  • Clarke CL, Therriault TW (2007) Biological synopsis of the invasive tunicate Styela clava (Herdman 1881). Can Man Rep Fish Aquat Sci 2807:23

    Google Scholar 

  • Coutts ADM, Taylor MD, Hewitt CL (2007) Novel method for assessing the en route survivorship of biofouling organisms on various vessel types. Mar Pollut Bull 54:97–116

    Article  PubMed  CAS  Google Scholar 

  • Dafforn KA, Glasby TM, Johnston EL (2008) Differential effects of tributyltin and copper antifoulants on recruitment of non-indigenous species. Biofouling 24:23–33

    Article  PubMed  CAS  Google Scholar 

  • Dafforn KA, Johnston EL, Glasby TM (2009) Shallow moving structures promote marine invader dominance. Biofouling 25:277–287

    Article  PubMed  CAS  Google Scholar 

  • Darbyson EA, Hanson JM, Locke A, Willison JHM (2009) Settlement and potential for transport of clubbed tunicate (Styela clava) on boat hulls. Aquat Invasion 4:95–103

    Article  Google Scholar 

  • Dark SJ (2004) The biogeography of invasive alien plants in California: an application of GIS and spatial regression analysis. Divers Distrib 10:1–9

    Article  Google Scholar 

  • Davidson IC, Zabin CJ, Chang AL, Brown CW, Sytsma MD, Ruiz GM (2010) Recreational boats as potential vectors of marine organisms at an invasion hotspot. Aquat Biol 11:179–191

    Article  Google Scholar 

  • Denny MW (1994) Extreme drag forces and the survival of wind- and water-swept organisms. J Exp Biol 194:97–115

    PubMed  Google Scholar 

  • Denny M (1995) Predicting physical disturbance: mechanistic approaches to the study of survivorship on wave-swept shores. Ecol Monogr 65:371–418

    Article  Google Scholar 

  • Denny MW, Gaylord B (2002) The mechanics of wave-swept algae. J Exp Biol 205:1355–1362

    PubMed  Google Scholar 

  • Edlund AF, Koehl MA (1998) Adhesion and reattachment of compound ascidians to various substrata: weak glue can prevent tissue damage. J Exp Biol 201:2397–2402

    PubMed  CAS  Google Scholar 

  • Epelbaum A, Herborg LM, Therriault TW, Pearce CM (2009) Temperature and salinity effects on growth, survival, reproduction, and potential distribution of two non-indigenous botryllid ascidians in British Columbia. J Exp Mar Biol Ecol 369:43–52

    Article  Google Scholar 

  • Evans SM, Birchenough AC, Brancato MS (2000) The TBT Ban: out of the frying pan into the fire? Mar Pollut Bull 40:204–211

    Article  CAS  Google Scholar 

  • Field D (1999) Disaster averted? Black striped mussel outbreak in northern Australia. Fish Farming Int 26:30–31

    Google Scholar 

  • Flagella MM, Verlaque M, Soria A, Buia MC (2007) Macroalgal survival in ballast water tanks. Mar Pollut Bull 54:1395–1401

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Floerl O, Pool TK, Inglis GJ (2004) Positive interactions between nonindigenous species facilitate transport by human vectors. Ecol Appl 14:1724–1736

    Article  Google Scholar 

  • Frey MA, Gartner HN, Clarke Murray C, Therriault TW (2009) First confirmed records of the non-native amphipod Caprella mutica (Schurin 1935) along the coast of British Columbia, Canada, and the potential for secondary spread via hull fouling. Aquat Invasion 4:495–499

    Article  Google Scholar 

  • Gaylord B (2000) Biological implications of surf-zone flow complexity. Limnol Oceanogr 45:174–188

    Article  Google Scholar 

  • Gaylord B, Blanchette CA, Denny MW (1994) Mechanical consequences of size in wave-swept algae. Ecol Monogr 64:287–313

    Article  Google Scholar 

  • Gollasch S, Lenz J, Dammer M, Andres H (2000) Survival of tropical ballast water organisms during a cruise from the Indian Ocean to the North Sea. J Plankton Res 22:923–937

    Article  Google Scholar 

  • Gosling EM, Wilkins NP (1981) Ecological genetics of the mussels Mytilus edulis and Mytilus galloprovincialis on Irish coasts. Mar Ecol Prog Ser 4:221–227

    Article  Google Scholar 

  • Herborg LM, O’Hara P, Therriault TW (2008) Forecasting the potential distribution of the invasive tunicate Didemnum vexillum. J Appl Ecol 46:64–72

    Article  Google Scholar 

  • Highsmith RC (1982) Reproduction by fragmentation by corals. Mar Ecol Prog Ser 7:207–226

    Article  Google Scholar 

  • Hilbish TJ, Carson EW, Plante JR, Weaver LA, Gilg MR (2002) Distribution of Mytilus edulis, M. galloprovincialis, and their hybrids in open-coast populations of mussels in southwestern England. Mar Biol 140:137–142

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hoppe KN (2002) Teredo navalis: the cryptogenic shipworm. In: Leppakoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe: distribution, impacts, and management. Springer, New York, pp 116–119

    Google Scholar 

  • Hunt HL, Scheibling RE (2001) Predicting wave dislodgment of mussels: variation in attachment strength with body size, habitat, and season. Mar Ecol Prog Ser 213:157–164

    Article  Google Scholar 

  • Johnson AS (2001) Drag, drafting, and mechanical interactions in canopies of the red alga Chondrus crispus. Biol Bull 201:126–135

    Article  PubMed  CAS  Google Scholar 

  • Johnson AS, Koehl MAR (1994) Maintenance of dynamic strain similarity and environmental stress factor in different flow habitats: Thallus allometry and material properties of a giant kelp. J Exp Biol 195:381–410

    PubMed  Google Scholar 

  • Johnson LE, Ricciardi A, Carlton JT (2001) Overland dispersal of aquatic invasive species: a risk assessment of transient recreational boats. Ecol Appl 11:1789–1799

    Article  Google Scholar 

  • Kado R (2003) Invasion of Japanese shores by the NE Pacific barnacle Balanus glandula and its ecological and biogeographical impact. Mar Ecol Prog Ser 249:199–206

    Article  Google Scholar 

  • Kitzes JA, Denny MW (2005) Red algae respond to waves: morphological and mechanical variation in Mastocarpus papillatus along a gradient of force. Biol Bull 208:114–119

    Article  PubMed  Google Scholar 

  • Koehl MAR (1984) How do benthic organisms withstand moving water? Am Zool 24:57–70

    Google Scholar 

  • Koehl MA (1999) Ecological biomechanics of benthic organisms: life history, mechanical design and temporal patterns of mechanical stress. J Exp Biol 202:3469–3476

    PubMed  CAS  Google Scholar 

  • Koehl MA (2000) Mechanical design and hydrodynamics of blade-like algae: Chondracanthus exasperatus. In: Spatz HC, Speck T (eds) Third international plant biomechanics conference. Thieme Verlag, Stuttgart, pp 295–308

    Google Scholar 

  • Koehl MA (2007) Mini review: hydrodynamics of larval settlement into fouling communities. Biofouling 23:359–369

    Article  Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  • Laird MC, Griffiths CL (2008) Present distribution and abundance of the introduced barnacle Balanus glandula Darwin in South Africa. Afr J Mar Sci 30:93–100

    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 

  • Lawson J, Davenport J, Whitaker A (2004) Barnacle distribution in Lough Hyne Marine Nature Reserve: a new baseline and an account of invasion by the introduced Australasian species Elminius modestus Darwin. Estuarine Coastal Shelf Sci 60:729–735

    Article  Google Scholar 

  • Levine JM, D’Antonio CM (2003) Forecasting biological invasions with increasing international trade. Conserv Biol 17:322–326

    Article  Google Scholar 

  • Locke A, Hanson JM, Ellis KM, Thompson J, Rochette J (2007) Invasion of the southern Gulf of St. Lawrence by the clubbed tunicate (Styela clava Herdman): potential mechanisms for invasions of Prince Edward Island estuaries. J Exp Mar Biol Ecol 342:69–77

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    Article  PubMed  Google Scholar 

  • Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–137

    Article  PubMed  CAS  Google Scholar 

  • Mach KJ, Nelson DV, Denny MW (2007) Techniques for predicting the lifetimes of wave-swept macroalgae: a primer on fracture mechanics and crack growth. J Exp Biol 210:2213–2230

    Article  PubMed  Google Scholar 

  • Mach KJ, Tepler SK, Staaf AV, Bohnhoff JC, Denny MW (2011) Failure by fatigue in the field: a model of fatigue breakage for the macroalga Mazzaella, with validation. J Exp Biol 214:1571–1585

    Article  PubMed  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 

  • Martone PT, Denny MW (2008a) To bend a coralline: effect of joint morphology on flexibility and stress amplification in an articulated calcified seaweed. J Exp Biol 211:3421–3432

    Article  PubMed  Google Scholar 

  • Martone PT, Denny MW (2008b) To break a coralline: mechanical constraints on the size and survival of a wave-swept seaweed. J Exp Biol 211:3433–3441

    Article  PubMed  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 

  • McMahon RF (2002) Evolutionary and physiological adaptations of aquatic invasive animals: r selection versus resistance. Can J Fish Aquat Sci 59:1235–1244

    Article  Google Scholar 

  • Padilla DK, Chotkowski MA, Buchan LA (1996) Predicting the spread of zebra mussels (Dreissena polymorpha) to inland waters using boater movement patterns. Glob Ecol Biogeogr Lett 5:353–359

    Article  Google Scholar 

  • Pawlik JR (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol Annu Rev 30:273–335

    Google Scholar 

  • Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803

    Article  PubMed  CAS  Google Scholar 

  • Pilsbry HA (1916) The sessile barnacles (Cirripedia) contained in the collections of the U.S. National Museum; including a monograph of the American species. Bull US Nat Mus 93:1–366

    Article  Google Scholar 

  • Piola RF, Johnston EL (2009) Comparing differential tolerance of native and non-indigenous marine species to metal pollution using novel assay techniques. Environ Pollut 157:2853–2864

    Article  PubMed  CAS  Google Scholar 

  • Piola RF, Dafforn KA, Johnston EL (2009) The influence of antifouling practices on marine invasions. Biofouling 25:633–644

    Article  PubMed  CAS  Google Scholar 

  • Schneider KR, Wethey DS, Helmuth BST, Hilbish TJ (2005) Implications of movement behavior on mussel dislodgment: exogenous selection in a Mytilus spp. hybrid zone. Mar Biol 146:333–343

    Article  Google Scholar 

  • Schultz MP, Kavanagh CJ, Swain GW (1999) Hydrodynamic forces on barnacles: implications on detachment from fouling-release surfaces. Biofouling 13:323–335

    Article  CAS  Google Scholar 

  • Schwindt E (2007) The invasion of the acorn barnacle Balanus glandula in the south-western Atlantic 40 years later. J Mar Bio Ass UK 87:1219–1225

    Google Scholar 

  • Skibinski DOF, Roderick EE (1991) Evidence of selective mortality in favor of the Mytilus galloprovincialis Lmk phenotype in British mussels. Biol J Linn Soc 42:351–366

    Article  Google Scholar 

  • Southward AJ, Burton RS, Coles SL, Dando PR, DeFelice R, Hoover J, Parnell PE, Tamaguchi T, Newman WA (1998) Invasion of Hawaiian shores by an Atlantic barnacle. Mar Ecol Prog Ser 165:119–126

    Article  Google Scholar 

  • Tyrell MC, Byers JEB (2007) Do artificial substrates favor nonindigenous fouling species over native species? J Exp Mar Biol Ecol 342:54–60

    Article  Google Scholar 

  • Utter BD, Denny MW (1996) Wave-induced forces on the giant kelp Macrocystis pyrifera (Agardh): field test of a computational model. J Exp Biol 199:2645–2654

    PubMed  Google Scholar 

  • Vogel S (1984) Drag and flexibility in sessile organisms. Am Zool 24:28–34

    Google Scholar 

  • Vogel S (2003) Comparative biomechanics: life’s physical world. Princeton University Press, Princeton

    Google Scholar 

  • Witman JD, Suchanek TH (1984) Mussels in flow: drag and dislodgment by epizoans. Mar Ecol Prog Ser 16:259–268

    Article  Google Scholar 

  • Worcester SE (1994) Adult rafting versus larval swimming: dispersal and recruitment of a botryllid ascidian on eelgrass. Mar Biol 121:309–317

    Article  Google Scholar 

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Acknowledgments

The authors wish to thank N. Backe, B. Claman, T. Goodman, M. Herborg, J. Nelson and C. Simkanin for field and laboratory assistance. We are grateful to Megan Mach for creating the illustrations in the manuscript. Detailed comments by L. Brown, K. Demes and two anonymous reviewers improved earlier versions of this manuscript. Conference travel support was provided by the Canadian Aquatic Invasive Species Network (CAISN). Research funding was provided by the Aquatic Invasive Species program of Fisheries & Oceans Canada as well as a Natural Sciences and Engineering Research Council (NSERC) Postgraduate Scholarship and a University of British Columbia (UBC) Affiliated Fellowship to CCM.

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Authors and Affiliations

  1. Department of Earth and Ocean Sciences, University of British Columbia, Vancouver, BC, Canada

    Cathryn Clarke Murray

  2. Pacific Biological Station, Fisheries and Oceans Canada, Nanaimo, BC, Canada

    Thomas W. Therriault

  3. Botany Department and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, Canada

    Patrick T. Martone

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  1. Cathryn Clarke Murray
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  2. Thomas W. Therriault
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Correspondence to Cathryn Clarke Murray.

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Clarke Murray, C., Therriault, T.W. & Martone, P.T. Adapted for invasion? Comparing attachment, drag and dislodgment of native and nonindigenous hull fouling species. Biol Invasions 14, 1651–1663 (2012). https://doi.org/10.1007/s10530-012-0178-0

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