Abstract
We developed a new predictive approach to evaluate the relative invasion hazard posed by recreational boats as vectors for non-indigenous species (NIS) in marine ecoregions on the Atlantic coast of Canada. It combines data from behavioral boater questionnaires, surveys of boat macrofouling, and an extensive NIS monitoring program in marinas. The relative invasion hazard posed by boats in nine marine ecoregions was estimated by combining information on NIS infestation levels in source ecoregions, the probability that boats will be fouled, boat movements and environmental similarity between source and receiving marinas, and estimates of annual recreational traffic within and between ecoregions. A total of 52.1% of surveyed boats had macrofouling on hull or niche areas, suggesting a high potential for NIS transport. High-risk boats were those that had spent extended periods in water, traveled extensively from invaded locations, and received little maintenance. Further, the high degree of connectivity between and within ecoregions, and high survival probabilities of NIS, highlight the threat of NIS introduction and spread via recreational boating in Atlantic Canadian waters. Of all Atlantic Canadian ecoregions, the Scotian Shelf ecoregion was classified as having the “Highest” Final Hazard score. However, boats with Intermediate to Highest scores travel to most ecoregions, underlining the importance of this vector to the introduction and spread of NIS in Atlantic Canadian coast. A simulated out-of-water cleaning after 3 months reduced the hazard in ecoregions with greater scores.
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References
Abell R, Thieme ML, Revenga C, Bryer M, Kottelat M, Bogutskaya N, Coad B, Mandrak N, Balderas SC, Bussing W, Stiassny MLJ, Skelton P, Allen GR, Unmack P, Naseka A, Ng R, Sindorf N, Robertson J, Armijo E, Higgins JV, Hebeil TJ, Wikrmanayake E, Olson E, Lopez HL, Reis RE, Lundberg JG, Pérez MHS, Petry P (2008) Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58(5):403–414. https://doi.org/10.1641/B580507
Acosta H, Forrest BM (2009) The spread of marine non-indigenous species via recreational boating: a conceptual model for risk assessment based on fault tree analysis. Ecol Model 220:1586–1598
Acosta H, Wu D, Forrest BM (2010) Fuzzy experts on recreational vessels, a risk modelling approach for marine invasions. Ecol Model 221:850–863
Aldred N, Clare AS (2014) Mini-review: impact and dynamics of surface fouling by solitary and compound ascidians. Biofouling 30:259–270
Ashton GV, Boos K, Shucksmith R, Cook EJ (2006) Risk assessment of hull fouling as a vector for marine non-natives in Scotland. Aquat Invasions 1(4):214–218. https://doi.org/10.3391/ai.2006.1.4.4
Ashton GV, Zabin C, Davidson I, Ruiz G (2012) aquatic invasive species vector risk assessments: recreational vessels as vectors for non-native marine species in California. Final report. July 2012. California Ocean Science Trust, USA
Barry SC, Hayes KR, Hewitt CL, Behrens HL, Dragsund E, Bakke SM (2008) Ballast water risk assessment: principles, processes, and methods. ICES J Mar Sci 65:121–131. https://doi.org/10.1093/icesjms/fsn004
Bird CJ, Dadswell MJ, Grund DW (1993) First record of the potential nuisance alga Codium fragile ssp. tomentosoides (Chlorophyta, Caulerpales) in Atlantic Canada. Proc NS Inst Sci 40:11–17
Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol Annu Rev 23:313–371
Carver CE, Mallet AL, Vercaemer B (2006) Biological synopsis of the colonial tunicates, Botryllus schlosseri and Botrylloides violaceus. Can Man Rep Fish Aquat Sci 2747:v + 42p
Clarke Murray C, Pakhamoz EA, Therriault TW (2011) Recreational boating: a large unregulated vector transporting marine invasive species. Divers Distrib 17:1161–1172. https://doi.org/10.1111/j.1472-4642.2011.00798.x
Clarke Murray C, Therriault TW, Martone P (2012) Adapted for invasion? Comparing attachment, drag and dislodgement of native and nonindigenous hull fouling species. Biol Invasions 14:1651–1663
Clarke Murray C, Therriault TW, Pakhomov E (2013) What lies beneath? An evaluation of rapid assessment tools for management of hull fouling. Environ Manag 52(2):374–384. https://doi.org/10.1007/s00267-013-0085-x
Clarke Murray C, Gartner H, Gregr EJ, Chan K, Pakhomov E, Therriault TW (2014) Spatial distribution of marine invasive species: environmental, demographic and vector drivers. Divers Distrib 20(7):824–836
Colautti RI, Bailey SA, van Overdijk CDA, Amundsen K, MacIsaac HJ (2006) Characterised and projected costs of nonindigenous species in Canada. Biol Invasions 8:45–59. https://doi.org/10.1007/s10530-005-0236-y
Darbyson E, Locke A, Hanson JM, Willison JHM (2009) Marine boating habits and the potential for spread of invasive species in the Gulf of St. Lawrence. Aquat Invasions 4:87–94. https://doi.org/10.3391/ai.2009.4.1.9
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. https://doi.org/10.3354/ab00302
Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. J Anim Ecol 77(4):802–813. https://doi.org/10.1111/j.1365-2656.2008.01390.x
Farrell P, Fletcher RL (2006) An investigation of dispersal of the introduced brown alga Undaria pinnatifida (Harvey) Suringar and its competition with some species on the man-made structures of Torquay Marina (Devon, UK). J Exp Mar Biol Ecol 334(2):236–243
Ferrario J, Marchini A, Borrelli P, Berzolari FG, Occhipinti-Ambrogi A (2016) A fuzzy ‘boater’ model to detect fouling and spreading risk of non-indigenous species by recreational boats. J Environ Manag 182:198–207. https://doi.org/10.1016/j.jenvman.2016.07.029
Floerl O, Inglis GJ (2003) Boat harbour design can exacerbate hull fouling. Austral Ecol 28:116–127. https://doi.org/10.1046/j.1442-9993.2003.01254.x
Floerl O, Inglis GJ (2005) Starting the invasion pathway: the interaction between source populations and human transport vectors. Biol Invasions 7:589–606. https://doi.org/10.1007/s10530-004-0952-8
Floerl O, Inglis GJ, Hayden BJ (2005) A risk-based predictive tool to prevent accidental introductions of nonindigenous marine species. Environ Manag 35(6):765–778. https://doi.org/10.1007/s00267-004-0193-8
Floerl O, Inglis GJ, Dey K, Smith A (2009) The importance of transport hubs in stepping-stone invasions. J Appl Ecol 46(1):37–45. https://doi.org/10.1111/j.1365-2664.2008.01540.x
Floerl O, Inglis GJ, Diettrich J (2016) Incorporating human behaviour into the risk–release relationship for invasion vectors: why targeting only the worst offenders can fail to reduce spread. J Appl Ecol 53:742–750. https://doi.org/10.1111/1365-2664.12609
Fofonoff PW, Ruiz GM, Steves B, Carlton JT (2003) In ships or on ships? Mechanisms of transfer and invasion for non-native species to the coasts of North America. In: Ruiz GM, Carlton JT (eds) Invasive species: vectors and management strategies. Island Press, Washington, pp 152–182
Gollasch S, Leppäkoski E (2007) Risk assessment and management scenarios for ballast water mediated species introductions into the Baltic Sea. Aquat Invasions 2(4):313–340. https://doi.org/10.3391/ai.2007.2.4.3
Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17(1):22–27. https://doi.org/10.1016/S0169-5347(01)02358-8
Harper JR, Christian J, Cross WE, Firth R, Searing G, Thompson D (1993) A classification of the marine regions of Canada—final report. Coastal and Oceans Resources Inc.
Hay CH (1990) The dispersal of sporophytes of Undaria pinnatifida by coastal shipping in New Zealand, and implications for further dispersal of Undaria in France. Br Phycol J 25:301–313
Hayes KR (2002) Identifying hazards in complex ecological systems. Part 2: infection modes and effects analysis for biological invasions. Biol Invasions 4:251–261
Kauano RV, Roper JJ, Rocha RM (2017) Small boats as vectors of marine invasions: experimental tests of velocity and desiccation as limits. Mar Biol 64:27. https://doi.org/10.1007/s00227-016-3057-x
Lacoursière-Roussel A, Bock DG, Cristescu M, Guichard F, Girard P, Legendre P, McKindsey CW (2012a) Disentangling invasion processes in a dynamic shipping-boating network. Mol Ecol 21:4227–4241. https://doi.org/10.1111/j.1365-294X.2012.05702.x
Lacoursière-Roussel A, Forrest BM, Guichard F, Piola RF, McKindsey CW (2012b) Modeling biofouling from boat and source characteristics: a comparative study between Canada and New Zealand. Biol Invasions 14:2301–2314. https://doi.org/10.1007/s10530-012-0230-0
Lacoursière-Roussel A, Bock DG, Cristescu ME, Guichard F, McKindsey CW (2016) Effect of shipping traffic on biofouling invasion success at population and community levels. Biol Invasions 18:1387–3547. https://doi.org/10.1007/s10530-016-1258-3
Lambert CC, Lambert G (1998) Non-indigenous ascidians in southern California harbors and marinas. Mar Biol 130(4):675–688. https://doi.org/10.1007/s002270050289
Lutzen J (1999) Styela clava Herdman (Urochordata, Ascidiacea) a successful immigrant to North West Europe: ecology, propagation and chronology of spread. Helgol Meeresun 52:383–391. https://doi.org/10.1007/BF02908912
Mandrak NE, Cudmore B, Chapman PM (2012) National detailed-level risk assessment guidelines: assessing the biological risk of aquatic invasive species in Canada. Can Sci Advis Sec Res Doc 2011/092:vi + 15 p
McGeoch MA, Genovesi P, Bellingham PJ, Costello MJ, McGrannachan C, Sheppard A (2016) Prioritizing species, pathways, and sites to achieve conservation targets for biological invasion. Biol Invasions 18:299–314. https://doi.org/10.1007/s10530-015-1013-1
McKenzie CH, Matheson K, Caines S, Wells T (2016) Surveys for non-indigenous tunicate species in Newfoundland, Canada (2006-2014): a first step towards understanding impact and control. Manag Biol Invasions 7(1):21–32. https://doi.org/10.3391/mbi.2016.7.1.04
McKindsey CW, Landry T, O’Beirn FX, Davies IM (2007) Bivalve aquaculture and exotic species: a review of ecological considerations and management issues. J Shellfish Res 26:281–294. https://doi.org/10.2983/0730-8000(2007)26%5b281:BAAESA%5d2.0.CO;2
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine diversity. Front Ecol Environ 6:485–492
Moore AM, Vercaemer B, DiBacco C, Sephton D, Ma KC (2014) Invading Nova Scotia: first records of Didemnum vexillum Kott, 2002 and four more non-indigenous invertebrates in 2012 and 2013. BioInvasions Rec 3(4):225–234. https://doi.org/10.3391/bir.2014.3.4.03
Pederson J, Bullock R, Carlton J, Dijkstra J, Dobroski N, Dyrynda P, Fisher R, Harris L, Hobbs N, Lambert G, Lazo-Wasem E, Mathieson A, Miglietta M-P, Smith III J, Tyrrell M (2006) Marine invaders in the Northeast: rapid assessment survey of non-native and native marine species of floating dock communities, August 2003. Massachusetts Institute of Technology Sea Grant Technical Reports, MITSG 05-03, i + 40p
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(6):621–632. https://doi.org/10.1093/icb/37.6.621
Sephton D, Vercaemer B, Nicolas JM, Keays J (2011) Monitoring for invasive tunicates in Nova Scotia, Canada (2006–2009). Aquat Invasions 6(4):391–403. https://doi.org/10.3391/ai.2011.6.4.04
Simard N, Pereira S, Estrada R, Nadeau M (2013) State of marine invasive species in Quebec. Can Manuscr Rep Fish Aquat Sci 3020:viii + 61 p
Simard Y, Roy N, Giard S, Yayla M (2014) Canadian year-round shipping traffic atlas for 2013: volume 1, East Coast marine waters. Can Tech Rep Fish Aquat Sci 3091(Vol.1)E:xviii + 327 pp
Simard N, Pelletier-Rousseau M, Clarke Murray C, McKindsey CW, Therriault TW, Lacoursière-Roussel A, Bernier R, Sephton D, Drolet D, Locke A, Martin JL, Drake DAR, McKenzie CH (2017) National Risk Assessment of Recreational Boating as a Vector for Marine Non-indigenous Species. DFO Can Sci Advis Sec Res Doc 2017/006:vi + 95 p
Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Gallil B, Garcia-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28(1):58–66. https://doi.org/10.1016/j.tree.2012.07.013
Sorte CJ, Williams SL, Carlton JT (2010) Marine range shifts and species introductions: comparative spread rates and community impacts. Glob Ecol Biogeogr 19(3):303–316. https://doi.org/10.1111/j.1466-8238.2009.00519.x
Spalding MD, Fox HE, Allen GR, Davidson N, Ferdeña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, MacManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57(7):573–583. https://doi.org/10.1641/B570707
Therriault TW, Herborg LM (2007) Risk assessment for two solitary and three colonial tunicates in both Atlantic and Pacific Canadian waters. Can Sci Advis Sec Res Doc 2007/063:64 p
Williams SL, Davidson IC, Pasari JR, Ashton GV, Carlton JT, Crafton RE, Fontana RE, Grosholz ED, Miller AW, Ruiz GM, Zabin CJ (2013) Managing multiple vectors for marine invasions in an increasingly connected world. Bioscience 63:952–966
Zhan A, Briski E, Bock DG, Ghabooli S, MacIsaac HJ (2015) Ascidians as models for studying invasion success. Mar Biol 162:2449–2470. https://doi.org/10.1007/s00227-015-2734-5
Acknowledgements
The authors wish to thank the laboratory and field assistants who helped in different aspects of this study: Isabelle Bérubé, Geneviève Perrin, Rafael Estrada, Sophie Boudreau, Benedikte Vercaemer, Murielle LeGresley, Paul McCurdy, Jocelyn Lowther, Terri Wells, Kyle Matheson, Robert O’Donnell, Andrew Perry, Mark O’Flaherty, George Bishop, Haley Lambert, Vanessa Reid, Erica Watson, André Nadeau, John Davidson, Colin Forsythe, Chantal Coomber, Janelle Mclaughlin, Emily White, Siobhan Curry, and Rod Asher. We are also grateful to Jessica Paulmert and Paul Couture for database development; to Vicky Yaroshewski and Pierre Clement who provided background data from the AIS Monitoring Database, Andrea Weise who prepared numerous maps and reviewed the document, and Émilie Simard and Marie-France Lavoie for their precious advice. Finally, we are very grateful to marina managers for allowing access to their facilities and boat owners for their participation. We thank the anonymous reviewers whose contribution helped to produce a better manuscript. This work was funded by the Fisheries and Oceans Canada Aquatic Invasive Species program. Additional funding was provided through the Canadian Aquatic Invasive Species Network (study by Lacoursière-Roussel) and the Newfoundland Provincial Department of Fisheries and Aquaculture. Lacoursière-Roussel was further supported by scholarships from McGill University, Québec-Océan and Fonds de recherche sur la nature et les technologies (FQRNT).
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Pelletier-Rousseau, M., Bernier, R., Clarke Murray, C. et al. Assessment of recreational boating as a vector for marine non-indigenous species on the Atlantic coast of Canada. Biol Invasions 21, 2447–2470 (2019). https://doi.org/10.1007/s10530-019-01991-1
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DOI: https://doi.org/10.1007/s10530-019-01991-1