Abstract
Propagule pressure (i.e., the frequency and abundance of introductions) is a common indicator of the likelihood of nonindigenous aquatic species (NAS) establishment success. Evaluating propagule pressure associated with multiple introduction pathways relative to present NAS distribution patterns may identify which pathway presents the greatest risk. Our objective was to develop and evaluate three geospatial metrics for the Laurentian Great Lakes as proxies of propagule pressure associated with three major introduction pathways: maritime commerce, organisms in trade, and water recreation. Logistic and linear regression analyses were conducted between NAS presence and introduction pathway intensity (e.g., number of vessel trips received by a port) for 23 NAS over a five-decade period (1970–2013). Notably, city population size was the best predictor of NAS presence, even for NAS introduced through ballast water discharge. Moreover, through time, city population size was an increasingly significant predictor of the presence of organisms in trade, signaling a change in both the types of organisms introduced and places where introductions are occurring. Nonetheless, all three metrics are reasonable proxies for propagule pressure and as such are applicable for risk assessment, monitoring, and control strategies.
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References
Allan, J. D., P. B. McIntyre, S. D. P. Smith, B. S. Halpern, G. L. Boyer, A. Buchsbaum, G. A. Burton, L. M. Campbell, W. L. Chadderton, J. J. H. Ciborowski, P. J. Doran, T. Eder, D. M. Infante, L. B. Johnson, C. A. Joseph, A. L. Marino, A. Prusevich, J. G. Read, J. B. Rose, E. S. Rutherford, S. P. Sowa & A. D. Steinman, 2013. Joint analysis of stressors and ecosystem services to enhance restoration effectiveness. PNAS 110: 372–377.
Ashton, G. V., K. Boos, R. Shucksmith & E. J. Cook, 2006. Rapid assessment of the distribution of marine non-native species in marinas in Scotland. Aquatic Invasions 1: 209–213.
Bailey, S. A., F. Chan, S. M. Ellis, J. E. Bronnenhuber, J. N. Bradie & N. Simard, 2012. Risk Assessment for Ship-mediated Introductions of Aquatic Nonindigenous Species to the Great Lakes and Freshwater St. Lawrence River. DFO Canadian Science Advisory Secretariat Doc. 2011/104 vi+224: 1–230.
Bonferroni, C. E. 1936. Teoria Statistica delle Classi e Calcolo delle Probabilita. Libreria internazionale Seeber.
Blackburn, T. M., P. Pyšek, S. Bacher, J. T. Carlton, R. P. Duncan, V. Jarošík, J. R. U. Wilson & D. M. Richardson, 2011. A Proposed unified framework for biological invasions. Trends in Ecology & Evolution 26: 333–339.
Bossenbroek, J. M., C. E. Kraft & J. C. Nekola, 2001. Prediction of long-distance dispersal using gravity models: zebra mussel invasions of inland lakes. Ecological Applications 11: 1778–1788.
Bradie, J., C. Chivers & B. Leung, 2013. Importing risk: quantifying the propagule pressure–establishment relationship at the pathway level. Diversity and Distribution 19: 1020–1030.
Branstrator, D. K., A. E. Beranek, M. E. Brown, L. K. Hembre & D. R. Engstrom, 2017. Colonization dynamics of the invasive predatory cladoceran, Bythotrephes longimanus, inferred from sediment records. Limnology and Oceanography 62: 1096–1110.
Carlton, J. T. & J. B. Geller, 1993. Ecological roulette: the global transportation of nonindigenous marine organisms. Science 261: 78–82.
Colautti, R. I. & H. J. MacIsaac, 2004. A neutral terminology to define ‘invasive’ species. Diversity and Distributions 10: 135–141.
Copp, G. H., L. Vilizzi & R. E. Gozlan, 2010. The demography of introduction pathways, propagule pressure and occurrences of non-native freshwater fish in England. Aquatic Conservation: Marine and Freshwater Ecosystems 20: 595–601.
Clarke Murray, C., H. Gartner, E. J. Gregr, K. Chan, E. Pakhomov & T. W. Therriault, 2014. Spatial distribution of marine invasive species: environmental, demographic, and vector drivers. Diversity and Distributions 20: 824–836.
Crooks, J. A., 2005. Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12: 316–329.
Davis, A. J. S. & J. A. Darling, 2017. Recreational freshwater fishing drives non-native aquatic species richness patterns at a continental scale. Diversity and Distributions 23: 692–702.
Duggan, I. C., C. A. M. Rixon & H. J. MacIsaac, 2006. Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biological Invasions 8: 377–382.
ESRI, 2014. ArcGIS Desktop: Release 10. Environmental Systems Research Institute, Redlands.
Foster, V., R. J. Giesler, A. Meriwether, W. Wilson, C. R. Nall & C. J. Cook, 2016. Marine Biology 163: 173.
Gertzen, E. & B. Leung, 2011. Predicting the spread of invasive species in an uncertain world: accommodating multiple vectors and gaps in temporal and spatial data for Bythotrephes longimanus. Biological Invasions 13: 2433–2444.
Gertzen, E., O. Familiar & B. Leung, 2008. Quantifying invasion Pathways: fish Introductions from the aquarium trade. Canadian Journal of Fisheries and Aquatic Science 65: 1265–1273.
Gutsch, M. & J. C. Hoffman, 2016. A review of Ruffe (Gymnocephalus cernua) life history in its native versus non-native range. Reviews in Fish Biology and Fisheries 26: 213–233.
Hensler, S. R. & D. J. Jude, 2007. Diel vertical migration of round goby Larvae in the Great Lakes. Journal of Great Lakes Research 33: 95–302.
Herborg, L. M., P. O’Hara & T. W. Therriault, 2009. Forecasting the potential distribution of the invasive Tunicate Didemnum vexillum. Journal of Applied Ecology 46: 64–72.
Holeck, K. T., E. L. Mills, H. J. MacIsaac, M. R. Dochoda, R. I. Colautti & A. Ricciardi, 2014. Bridging troubled waters: biological invasions, transoceanic shipping, and the Laurentian Great Lakes. BioScience 54: 919–929.
Hoffman, J. C., J. R. Kelly, A. S. Trebitz, G. S. Peterson & C. W. West, 2011. Effort and potential efficiencies for aquatic non-native species early detection. Canadian Journal of Fisheries and Aquatic Sciences 68: 2064–2079.
Hoffman, J. C., J. Schloesser, A. S. Trebitz, G. S. Peterson, M. Gutsch, H. Quinlan & J. R. Kelly, 2016. Sampling design for early detection of aquatic invasive species in Great Lakes ports. Fisheries 41: 26–37.
Kolar, C. S. & D. M. Lodge, 2001. Progress in invasion biology: predicting invaders. Trends in Ecology and Evolution 16: 199–204.
Lapointe, N. W. R., P. L. Fuller, M. Neilson, B. R. Murphy & P. L. Angermeier, 2016. Pathways of fish invasion in the Mid-Atlantic region of the United States. Management of Biological Invasions 7: 221–233.
Leprieur, F., O. Beauchard, S. Blanchet, T. Oberdorff & S. Brosse, 2008. Fish invasions in the World’s River Systems: when natural processes are blurred by human activities. PLOS Biology 6(2): e28.
Leung, B., J. M. Drake & D. M. Lodge, 2004. Predicting invasions: propagule pressure and the gravity of Allee effects. Ecology 85: 1651–1660.
Lo, V. B., C. D. Levings & K. M. A. Chan, 2012. Quantifying potential propagule pressure of aquatic invasive species from the commercial shipping industry in Canada. Marine Pollution Bulletin 64: 295–302.
Lockwood, J. L., P. Cassey & T. M. Blackburn, 2009. The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Diversity and Distributions 15: 904–910.
Lodge, D. M., S. Williams, H. J. MacIsaac, K. R. Hayes, B. Leung, S. Reichard, R. N. Mack, P. B. Moyle, M. Smith, D. A. Andow, J. T. Carlton & A. McMichael, 2006. Biological invasions: recommendations for U.S. Policy and Management. Ecological Applications 16: 2035–2054.
Mackie, G. L. & D. W. Schlosser, 1996. Comparative biology of zebra mussels in Europe and North America: an overview. American Zoologist 36: 244–258.
Mills, E. L., J. H. Leach, J. T. Carlton & C. L. Secor, 1993. Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. Journal of Great Lakes Research 19: 1–54.
Molnar, J. L., R. L. Gamboa, C. Revenga & M. D. Spalding, 2008. Assessing the global threat of invasive species to marine biodiversity. Frontiers in Ecology and the Environment 6: 485–492.
Moran, P. A. P., 1948. The interpretation of statistical maps. Journal of the Royal Statistical Society 2: 243–251.
National Ballast Information Clearinghouse, 2015. NBIC Online Database. Electronic publication, Smithsonian Environmental Research Center & United States Coast Guard. Available from http://invasions.si.edu/nbic/search.html. Accessed 2 May 2015.
Padilla, D. K. & S. L. Williams, 2004. Beyond Ballast Water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Frontiers in Ecology and the Environment 2: 131–138.
Phillips, S. J., M. Dudik, C. H. Graham, A. Lehmann, J. Leathwick & S. Ferrier, 2009. Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. Ecological Applications 19: 181–197.
R Core Team, 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
Rao, Y. R. & D. J. Schwab, 2007. Transport and mixing between the coastal and offshore waters in the Great Lakes: a review. Journal of Great Lakes Research 33: 202–218.
Ray, W. J. & L. D. Corkum, 2001. Habitat and site affinity of the round goby. Journal of Great Lakes Research 27: 329–334.
Ricciardi, A., 2001. Facilitative interactions among aquatic invaders: is an “invasional meltdown” occurring in the Great Lakes? Canadian Journal of Fisheries and Aquatic Science 58: 2513–2525.
Ricciardi, A., 2006. Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Diversity and Distributions 12: 425–433.
Rilov, G., Y. Benayahu & A. Gasith, 2004. Prolonged lag in population outbreak of an invasive mussel: a shifting-habitat model. Biological Invasions 6: 347–364.
Rothlisberger, J. D. & D. M. Lodge, 2013. The Laurentian Great Lakes as a beachhead and a gathering place for biological invasions. Aquatic Invasions 4: 361–374.
Rup, M. P., S. A. Bailey, C. J. Wiley, M. S. Minton, A. W. Miller, G. M. Ruiz & H. J. MacIsaac, 2010. Domestic Ballast operations on the Great Lakes: potential importance of lakers as a vector for introduction and spread of nonindigenous species. Canadian Journal of Fisheries and Aquatic Science 67: 256–268.
Sala, O. E., F. S. Chapin III, J. J. Armesto, E. Berlow, J. Bloomfield, R. Dirzo, E. Huber-Sanwald, L. F. Huennek, R. B. Jackson, A. Kinzig, R. Leemans, D. M. Lodge, H. A. Mooney, M. Oesterheld, N. L. Poff, M. T. Sykes, B. H. Walker, M. Walker & D. H. Wall, 2000. Global biodiversity scenarios for the year 2100. Science 287: 1770–1774.
Seebens, H., N. Schwartz, P. J. Schupp, & B. Blasius, 2016. Predicting the Spread of Marine Species Introduced by Global Shipping. PNAS 113: 5646–5651.
Sieracki, J. L., J. M. Bossenbroek & W. L. Chadderton, 2014. A Spatial modeling approach to predicting the secondary spread of invasive species due to Ballast Water discharge. PLOS One. https://doi.org/10.1371/journal.pone.0114217.
Spalding, M. D., H. E. Fox, G. R. Allen, N. Davidson, Z. A. Ferdana, M. Finlayson, B. S. Halpern, M. A. Jorge, A. Lombana, S. A. Lourie, K. D. Martin, E. McManus, J. Molnar, C. A. Recchia, & J. Robertson, 2007. Marine Ecoregions of the World: A Bioregionalization of Coastal and Shelf Areas. BioScience 57: 573–583.
Statistics Canada. http://www12.statcan.gc.ca/census-recensement/index-eng.cfm. Accessed 2 May 2015.
Trebitz, A. S. J. R., J. C. Kelly, G. S. Peterson Hoffman & C. W. West, 2009. Exploiting habitat and gear patterns for efficient detection of rare and non-native benthos and fish in Great Lakes coastal ecosystems. Aquatic Invasions 4: 651–667.
U.S. Army Corps of Engineers, 2014. http://www.navigationdatacenter.us/data/datappor.htm. Accessed 2 May 2015.
U.S. Census Bureau. www.census.gov. Accessed 2 May 2015.
U.S. Geological Survey. Nonindigenous Aquatic Species database. http://nas.er.usgs.gov Accessed 2/5/2015.
Uzarski, D. G., V. J. Brady, M. J. Cooper, D. A. Wilcox, D. A. Albert, R. P. Axler, P. Bostwick, T. N. Brown, J. J. H. Ciborowski, N. P. Danz, J. P. Gathman, T. M. Gehring, G. P. Grabas, A. Garwood, R. W. Howe, L. B. Johnson, G. A. Lamberti, A. H. Moerke, B. A. Murry, G. J. Niemi, C. J. Norment, C. R. Ruetz III, A. D. Steinman, D. C. Tozer, R. Wheeler, T. K. O’Donnell & J. P. Schneider, 2017. Standardized measures of coastal wetland condition: implementation at a Laurentian Great Lakes basin-wide scale. Wetlands 37: 15–32.
von Holle, B. V. & D. Simberloff, 2005. Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86: 3212–3218.
Wells, M. G., S. A. Bailey & B. Ruddick, 2011. The dilution and dispersion of ballast water discharge in Goderich harbor. Marine Pollution Bulletin 62: 1288–1296.
Wonham, M., J. E. Byers, E. D. Grosholz & B. Leung, 2013. Modeling the relationship between propagule pressure and invasion risk to inform policy and management. Ecological Applications 23: 1691–1706.
Yurista, P. M. & J. R. Kelly, 2009. Spatial patterns of water quality and plankton from high-resolution continuous in situ sensing along a 537-km nearshore transect of western Lake Superior, 2004. In Munawar, M. & R. Heath (eds), State of Lake Superior. Aquatic Ecosystem Health and Management Society, Burlington: 439–471.
Acknowledgements
We thank Rochelle Sturtevant and Matt Cannister for providing nonindigenous aquatic species detection records from GLANSIS and the USGS NAS databases, Valerie Brady for providing nonindigenous aquatic invertebrate detections from the Great Lakes Indicator Consortium’s Coastal Wetlands Monitoring project, and David Allan, Sigrid Smith, Christine Joseph, and Sarah Bailey for providing marina size and ballast water discharge data from the Great Lakes Environmental Assessment and Mapping (GLEAM) project. The views expressed in this article are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency. This is Contribution # 622 of the University of Minnesota’s Natural Resources Research Institute publication series.
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Guest editors: John E. Havel, Sidinei M. Thomaz, Lee B. Kats, Katya E. Kovalenko & Luciano N. Santos / Aquatic Invasive Species II
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10750_2018_3551_MOESM1_ESM.tif
Supplemental Fig 1 Cumulative NAS detections grouped by decade from 1970 to 2013. Total detections per decade are displayed in the upper right corner of each panel. Each detection is represented by a closed black circle. Detections were included in a decade if they occurred between the 1st of January and the 31st of December, i.e. detections in the 1970s decade were from Jan. 1 1970 to Dec. 31 1979. We employed an assumption that after the initial detection, the species was treated as if it persisted from one decade to the next from the earliest detection onward. Supplementary material 1 (TIFF 1192 kb)
10750_2018_3551_MOESM2_ESM.tif
Supplemental Fig 2 Method for delineating areas of pathway influence (API). Port and marina pathway locations were merged based on buffer distances. Buffers were applied to pathway locations, and if overlap occurred (A), the areas of pathway influence (API) were merged, and all associated attributes of pathway intensity were summed together (B). The buffer distance for ports and cities was 10km; the marina buffer was 1km. To maintain discrete areas, cities APIs were not merged under any circumstances (C). If overlap would occur for two city API, the border between the two became the dividing line. Supplementary material 2 (TIFF 1602 kb)
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Supplemental Fig 3 Method for delineated composite APIs. For multiple logistic analyses, APIs had to be categorized into all possible combinations of the three pathway APIs. When spatial overlap of the individual APIs occurred, a new multivariable API was created with all the associated intensity metrics of the underlying APIs. If only two pathway APIs overlapped, the metric for the third pathway was assigned a zero value. Supplementary material 3 (TIFF 1296 kb)
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Supplemental Table 1 Comparison of commercial boat traffic simple logistic regression models. Significance was determined at a = 0.01; there were no significant relationships in the aquaria species models (omitted). Model fit values (-2*log(likelihood)) are displayed for significant results (*); p-values are displayed for non-significant results. ‘NV’ indicates that the analysis had no variation. Trips were categorized as discharging and non-discharging ballast water. Cargo was categorized into domestic (U.S. and Canada) and foreign origins. Highly invaded ports were defined as the top quartile ports for NAS richness (>7 species). Supplementary material 4 (TIFF 603 kb)
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O’Malia, E.M., Johnson, L.B. & Hoffman, J.C. Pathways and places associated with nonindigenous aquatic species introductions in the Laurentian Great Lakes. Hydrobiologia 817, 23–40 (2018). https://doi.org/10.1007/s10750-018-3551-x
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DOI: https://doi.org/10.1007/s10750-018-3551-x
Keywords
- Ballast water
- Live release
- Marinas
- Population size
- Propagule pressure