Abstract
Preventing the introduction of nonindigenous species (NIS) is the most efficient way to avoid the costs and impacts of biological invasions. The transport of fouling species on ship hulls is an important vector for the introduction of marine NIS. We use quantitative risk screening techniques to develop a predictive tool of the abundance and variety of organisms being transported by ocean-going yachts. We developed and calibrated an ordinal rank scale of the abundance of fouling assemblages on the hulls of international yacht hulls arriving in New Zealand. Fouling ranks were allocated to 783 international yachts that arrived in New Zealand between 2002 and 2004. Classification tree analysis was used to identify relationships between the fouling ranks and predictor variables that described the maintenance and travel history of the yachts. The fouling ranks provided reliable indications of the actual abundance and variety of fouling assemblages on the yachts and identified most (60%) yachts that had fouling on their hulls. However, classification tree models explained comparatively little of the variation in the distribution of fouling ranks (22.1%), had high misclassification rates (∼43%), and low predictive power. In agreement with other studies, the best model selected the age of the toxic antifouling paint on yacht hulls as the principal risk factor for hull fouling. Our study shows that the transport probability of fouling organisms is the result of a complex suite of interacting factors and that large sample sizes will be needed for calibration of robust risk models.
Similar content being viewed by others
Literature Cited
AMOG Consulting. 2002. Hull fouling as a vector for the translocation of marine organisms. Phase I: Hull fouling research. Ballast water research series, Report no. 14. Department of Agriculture, Fisheries and Forestry Australia, Canberra, 142 pp
N. Bax J. T. Carlton A. Matthews-Amos R. L. Haedrich F. G. Howarth J. E. Purcell A. Rieser A. Gray (2001) ArticleTitleThe control of biological invasions in the world’s oceans Conservation Biology 15 1234–1246 Occurrence Handle10.1046/j.1523-1739.2001.99487.x
C. J. Bird M. J. Dadswell D. W. Grund (1993) ArticleTitleFirst record of the potential nuisance alga Codium fragile ssp. tomentosoides (Chlorophyta, Caulerpales) in Atlantic Canada Proceedings of the Nova Scotian Institute of Science 40 11–17
L. Breiman J. H. Freidman R. A. Olshen C. J. Stone (1984) Classification and regression trees Wadsworth Belmont 358
J. T. Carlton (1985) ArticleTitleTransoceanic and interoceanic dispersal of coastal marine organisms: The biology of ballast water Oceanography and Marine Biology Annual Reviews 23 313–371
J. T. Carlton J. B. Geller (1993) ArticleTitleEcological roulette: the global transport of nonindigenous marine organisms Science 261 78–81
J. T. Carlton J. A. Scanlon (1985) ArticleTitleProgression and dispersal of an introduced alga: Codium fragile ssp. tomentosoides (Chlorophyta) on the Atlantic coast of North America Botanica Marina 28 155–165
A. O. Christie R. Dalley (1987) Barnacle fouling and its prevention A. J. Southward (Eds) Barnacle biology A.A. Balkema Rotterdam 419–433
Coutts, A. D. M. 1999. Hull fouling as a modern vector for marine biological invasions: investigation of merchant vessels visiting northern Tasmania. M.App.Sc. thesis. Australian Maritime College, Tasmania, 283 pp
Cranfield, H. J., D. P. Gordon, R. C. Willan, B. A. Marshall, C. N. Battershill, M. P. Francis, W. A. Nelson, C. J. Glasby, and G. B. Read. 1998. Adventive marine species in New Zealand. National Institute of Water and Atmospheric Research Technical Report 34. Wellington, 48 pp.
G. De’ath K. E. Fabricius (2000) ArticleTitleClassification and regression trees: A powerful yet simple technique for ecological data analysis Ecology 81 3178–3192
L. G. Eldredge J. T. Carlton (2002) ArticleTitleHawaiian marine bioinvasions: A preliminary assessment Pacific Science 56 211–212
D. Field (1999) ArticleTitleDisaster averted? Black striped mussel outbreak in northern Australia Fish Farming International 26 30–31
R. L. Fletcher P. Farrell (1998) ArticleTitleIntroduced brown algae in the North East Atlantic, with particular respect to Undaria pinnatifida (Harvey) Suringar Helgolander Meeresuntersuchungen 52 259–275
O. Floerl (2002) Intracoastal spread of fouling organisms by recreational vessels. PhD thesis James Cook University Townsville 283
O. Floerl G. J. Inglis (2003) ArticleTitleBoat harbour design can exacerbate hull fouling Austral Ecology 28 116–127 Occurrence Handle10.1046/j.1442-9993.2003.01254.x
O. Floerl G. J. Inglis B. J. Hayden (2003) ArticleTitleBiosecurity “HullCam” Ballast Water News 14 8
Floerl, O., and G. J. Inglis. Starting the invasion pathway: the interaction between source populations and human transport vectors. Biological Invasions. In press
Floerl, O., G. J. Inglis, and H. M. Marsh. Selectivity in vector management: An investigation of the effectiveness of measures used to prevent transport of non-indigenous species. Biological Invasions. In press
S. Gollasch (2002) ArticleTitleThe importance of ship hull fouling as a vector of species introductions into the North Sea Biofouling 18 105–121 Occurrence Handle10.1080/08927010290011361
I.A. Grigorovich R.I. Colautti E.L. Mills K. Holeck A. G. Ballert H. J. MacIsaac (2003) ArticleTitleBallast-mediated animal introductions in the Laurentian Great Lakes: Retrospective and prospective analyses Canadian Journal of Fisheries and Aquatic Sciences 60 740–756 Occurrence Handle10.1139/f03-053
A. Guisan N. E. Zimmermann (2000) ArticleTitlePredictive habitat distribution models in ecology Ecological Modelling 135 147–186 Occurrence Handle10.1016/S0304-3800(00)00354-9
C. H. Hay (1990) ArticleTitleThe dispersal of sporophytes of Undaria pinnatifida by coastal shipping in New Zealand, and implications for further dispersal of Undaria in France British Phycological Journal 25 301–313
K. R. Hayes (2003) Biosecurity and the role of risk assessment G. Ruiz J. T. Carlton (Eds) Invasive species: vectors and management strategies Island Press Washington, D. C., 382–414
K. R. Hayes C. L. Hewitt (2000) Quantitative biological risk assessment of the ballast water vector: An Australian approach J. Pederson (Eds) Marine Bioinvasions: Proceedings of the First National Conference Massachusetts Institute of Technology Cambridge, 370–386
R. Hengeveld (1999) Modelling the impact of biological invasions O. T. Sandlund P. J. Schei A. Viken (Eds) Invasive species and biodiversity management Kluwer Academic Publishers Dordrecht 127–138
Hewitt, C. L., M. L. Campbell, R. E. Thresher, and R. B. Martin. 1999. Marine biological invasions of Port Phillip Bay, Victoria. Centre for Research on Introduced Marine Pests technical report no. 20. CSIRO Marine Research, Hobart, 344 pp
D. W. Hosmer S. Lemeshow (1989) Applied logistic regression John Wiley and Sons New York, 307 pp
Hunter, J. E., and C. D. Anderson. 2001. Antifouling paints and the environment. International Marine Coatings technical paper. Available online at: http://www.international-marine.com/
G. J. Inglis (2001) Criteria for selecting New Zealand ports and other points of entry that have a high risk of invasion by new exotic marine organisms. Report prepared for the New Zealand Ministry of Fisheries National Institute of Water and Atmospheric Research Christchurch, 27 pp
P. James B. J. Hayden (2000) The potential for the introduction of exotic species by vessel hull fouling: A preliminary study. NIWA client report no. WLG 00/51 National Institute of Water and Atmospheric Research Wellington, 61 pp
P. T. Jenkins (1999) Trade and exotic species introductions O. T. Sandlund P. J. Schei A. Viken (Eds) Invasive species and biodiversity management Kluwer Academic Publishers Dordrecht, 229–235
M. J. Keough P. T. Raimondi (1995) ArticleTitleResponses of settling invertebrate larvae to bioorganic films: Effects of different types of films Journal of Experimental Marine Biology and Ecology 185 235–253 Occurrence Handle10.1016/0022-0981(94)00154-6
C. S. Kolar D. M. Lodge (2002) ArticleTitleEcological predictions and risk assessment for alien fishes in North America Science 298 1233–1236 Occurrence Handle10.1126/science.1075753 Occurrence Handle1:CAS:528:DC%2BD38XosVerurg%3D Occurrence Handle12424378
B. Leung D. M. Lodge D. Finnoff J. F. Shogren M. A. Lewis G. Lamberti (2002) ArticleTitleAn ounce of prevention or a pound of cure: Bioeconomic risk analysis of invasive species Proceedings of the Royal Society of London, Series B 269 2407–2413
J. M. Levine C. M. D’Antonio (2003) ArticleTitleForecasting biological invasions with increasing international trade Conservation Biology 17 322–326 Occurrence Handle10.1046/j.1523-1739.2003.02038.x
R. N. Mack D. Simberloff W. M. Lonsdale H. Evans M. Clout F. A. Bazzaz (2000) ArticleTitleBiotic invasions: Causes, epidemiology, global consequences, and control Ecological Applications 10 689–710
M. P. Marchetti P. B. Moyle R. Levine (2004) ArticleTitleAlien fishes in California watersheds: Characteristics of successful and failed invaders Ecological Applications 14 587–596
Marine Science and Ecology. 2002. Hull fouling as a vector for the translocation of marine organisms. Phase III: The significance of the prospective ban on tributyltin antifouling paints on the introduction and translocation of marine pests in Australia. Ballast water research series, report no. 15. Department of Agriculture, Fisheries and Forestry Australia, Canberra, 133 pp
Murphy, N. E., and B. Schaffelke. 2003. Caulerpa taxifolia in Australia: A growing problem. Page 96 in Proceedings of the Third International Conference on Marine Bioinvasions, La Jolla, California
Neil K. M. 2002. Asian green mussel and Caribbean tubeworm survey within proposed dredge areas. Queensland Department of Primary Industries Northern Fisheries Centre and CRC Reef Research Centre, Cairns, 10 pp
Rao, K. S., V. V. Srinivasan, and M. Balaji. 1989. Success and spread of the exotic fouling bivalve Mytilopsis sallei (Recluez) in Indian waters. pp 125–127 in Exotic species in India. Asian Fisheries Society, Mangalore
S. H. Reichard C. W. Hamilton (1997) ArticleTitlePredicting invasions of woody plants introduced into North America Conservation Biology 11 193–203 Occurrence Handle10.1046/j.1523-1739.1997.95473.x
M. Rejmánek (2000) ArticleTitleInvasive plants: approaches and predictions Austral Ecology 25 497–506 Occurrence Handle10.1046/j.1442-9993.2000.01080.x
M. Rejmánek D. M. Richardson (1996) ArticleTitleWhat attributes make some plant species more invasive? Ecology 77 1655–1660
A. Ricciardi H. J. MacIsaac (2000) ArticleTitleRecent mass invasion of the North American Lakes by Ponto-Caspian species Trends in Ecology and Evolution 15 62–65 Occurrence Handle10.1016/S0169-5347(99)01745-0 Occurrence Handle10652557
J. L. Ruesink I. M. Parker M. J. Groom P. M. Kareiva (1995) ArticleTitleReducing the risk of nonindigenous species introductions BioScience 45 465–477
G. M. Ruiz P. W. Fofonoff J. T. Carlton M. J. Wonham A. H. Hines (2000) ArticleTitleInvasion of coastal marine communities in North America: apparent patterns, processes, and biases Annual Reviews in Ecology and Systematics 31 481–531 Occurrence Handle10.1146/annurev.ecolsys.31.1.481
A. K. Sakai F. W. Allendorf J. S. Holt D. M. Lodge J. Molofsky K. A. With S. Baughman R. J. Cabin J. E. Cohen N. C. Ellstrand D. E. McCauley P. O’Neil I. M. Parker J. N. Thompson S. G. Weller (2001) ArticleTitleThe population biology of invasive species Annual Review of Ecology and Systematics 32 305–332 Occurrence Handle10.1146/annurev.ecolsys.32.081501.114037
D. Secord (2003) ArticleTitleBiological control of marine invasive species: cautionary tales and land-based lessons Biological Invasions 5 117–131 Occurrence Handle10.1023/A:1024054909052
L. D. Smith M. J. Wonham L. D. McCann G. M. Ruiz A. H. Hines J. T. Carlton (1999) ArticleTitleInvasion pressure to a ballast-flooded estuary and an assessment of inoculant survival Biological Invasions 1 67–87 Occurrence Handle10.1023/A:1010091918466
Steinberg D., D. Colla. 2000. Logistic regression. Pages 549–616 in Systat 10: Statistics I. SPPS Inc., New York
E. Steinke (1999) The Australian Quarantine and Inspection Service weed risk assessment system for new plant imports: Its development and implementation A. C. Bishop (Eds) 12th Australian Weeds Conference, papers and proceedings Tasmanian Weed Society Hobart
R. E. Thresher C. L. Hewitt M. L. Campbell (1999) Introduced and cryptogenic species in Port Phillip Bay C. L. Hewitt M. L. Campbell R. E. Thresher R. B. Martin (Eds) Marine Biological Invasions of Port Phillip Bay, Victoria Centre for Research on Introduced Marine Pests technical report no. 20. CSIRO Marine Research Hobart, 283–295
C. D. Todd M. J. Keough (1994) ArticleTitleLarval settlement in hard substratum epifaunal assemblages: A manipulative field study of the effects of substratum filming and the presence of incumbents Journal of Experimental Marine Biology and Ecology 181 159–187 Occurrence Handle10.1016/0022-0981(94)90126-0
M. J. Wonham J. T. Carlton G. M. Ruiz L. D. Smith (2000) ArticleTitleFish and ships: Relating dispersal frequency to success in biological invasions Marine Biology 136 1111–1121 Occurrence Handle10.1007/s002270000303
M. J. Wonham W. C. Walton G. M. Ruiz A. M. Frese B. S. Galil (2001) ArticleTitleGoing to the source: Role of the invasion pathway in determining potential invaders Marine Ecology Progress Series 215 1–12
Acknowledgments
We thank Kevin Kennett (MAF Quarantine Service) for facilitating the involvement of the Ministry of Agriculture and Forestry in this collaborative study. Special thanks to the MAF Quarantine officers who collected data on nearly 800 international yachts arriving in New Zealand: Mike Cartwright, Brian Whimp, and Peter Lord (Opua and Whangarei), Grant Weston (Tauranga), and Neville Moore (Auckland). Thanks are also due to Nick Gust, Crispin Middleton, and Matt Smith for their help in the field during the calibration of the HullCam, and to the Opua, Town Basin, Westhaven, Bayswater, and Gulf Harbour marinas in Opua, Whangarei, and Auckland for their support of this work. Ton Snelder, Drew Lohrer, David Secord, and two anonymous reviewers provided helpful comments on an earlier manuscript. This study was funded by NIWA NSOF projects PDEA035, NPDA045, and NNRY045.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Floerl, O., Inglis, G.J. & Hayden, B.J. A Risk-Based Predictive Tool to Prevent Accidental Introductions of Nonindigenous Marine Species. Environmental Management 35, 765–778 (2005). https://doi.org/10.1007/s00267-004-0193-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00267-004-0193-8