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Human-mediated and natural dispersal of an invasive fish in the eastern Great Lakes

Heredityvolume 120pages533546 (2018) | Download Citation


The globally invasive Round Goby (Neogobius melanostomus) was introduced to the Great Lakes around 1990, spreading widely and becoming the dominant benthic fish in many areas. The speed and scope of this invasion is remarkable and calls into question conventional secondary spread models and scenarios. We utilized nine microsatellites to identify large-scale genetic structure in Round Goby populations in the eastern Great Lakes, and assessed the role of colonization vs. secondary transport and dispersal in developing this structure. We identified three clusters, corresponding with Lake Huron, eastern Lake Erie, and western Lake Erie plus eastern Lake Ontario, along with three highly divergent populations. Bottleneck analysis identified founder effects in two divergent populations. Regression analyses of isolation by distance and allelic richness vs. distance from the initial invasion site were consistent with limited migration. However, some populations in eastern Lake Erie and Lake Ontario showed anomalously low genetic distance from the original site of colonization, consistent with secondary transport of large numbers of individuals via ballast water. We conclude that genetic structure of Round Goby in the Great Lakes principally resulted from long-distance secondary transport via ballast water with additional movement of individual via bait buckets and natural dispersal. The success of Round Gobies represents an interesting model for colonization characterization; however, those same attributes present significant challenges for conservation and fisheries management. Current management likely prevents many new species from arriving in the Great Lakes, but fails to address the transport of species within the lakes after they arrive; this is an issue of clear and pressing importance.

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  1. Alberto F, Arnaud-Haond S, Duarte CM, Serrão EA (2006) Genetic diversity of a clonal angiosperm near its range limit: the case of Cymodocea nodosa at the Canary Islands. Mar Ecol Prog Ser 309:117–129.

  2. Azour F, van Deurs M, Behrens J, Carl H, Hüssy K, Greisen K, Ebert R, Møller PR (2015) Invasion rate and population characteristics of the Round Goby Neogobius melanostomus: effects of density and invasion history. Aquat Biol 24:41–52.

  3. Britton JR, Gozlan RE (2013) Geo-politics and freshwater fish introductions: how the cold war shaped Europe’s fish allodiversity. Glob Environ Chang 23:1566–1574.

  4. Bronnenhuber JE, Dufour BA, Higgs DM, Heath DD (2011) Dispersal strategies, secondary range expansion and invasion genetics of the nonindigenous Round Goby, Neogobius melanostomus, in Great Lakes tributaries. Mol Ecol 20:1845–1859.

  5. Brown JH, Sax DF (2004) An essay on some topics concerning invasive species. Austral Ecol 29:530–536.

  6. Brown JE, Stepien CA (2009) Invasion genetics of the Eurasian Round Goby in North America: tracing sources and spread patterns. Mol Ecol 18:64–79.

  7. Buchan LAJ, Padilla DK (1999) Estimating the probability of long-distance overland dispersal of invading aquatic species. Ecol Appl 9:254–265.

  8. Canadian Coast Guard (1989) Voluntary guidelines for the control of ballast water discharges from ships proceeding to the St. Lawrence River and Great Lakes. Government of Canada, Ottawa, ON.

  9. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631.

  10. Colautti RI, Niimi AJ, Van Overdijk CDA, Mills EL, Holeck K, MacIsaac HJ (2003) Spatial and temporal analysis of transoceanic shipping vectors to the Great Lakes. In: Ruiz GM, Carlton JT(eds)Invasive species: vectors and management strategies. Island Press, Washington, DC, 227–246.

  11. Corkum LD, MacInnis AJ, Wickett RG (1998) Reproductive habits of Round Gobies. Gt Lakes Res Rev 3:13–20.

  12. Corkum LD, Sapota MR, Skora KE (2004) The Round Goby, Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean. Biol Invasions 6:173–181.

  13. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014.

  14. Crossman EJ, Holm E, Cholmondeley R, Tuininga K (1992) First record for Canada of the Rudd, Scardinius erythrophthalmus, and notes on the introduced Round Goby, Neogobius melanostomus. Can Field-Nat 106:206–209.

  15. DAISIE (2017) Delivering Alien Invasive Species Inventories for Europe.

  16. Dufour BA, Hogan TM, Heath DD (2007) Ten polymorphic microsatellite markers in the invasive Round Goby (Neogobius melanostomus) and cross-species amplification. Mol Ecol Notes 7:1205–1207.

  17. Elphinstone MS, Hinten GN, Anderson MJ, Nock CJ (2003) An inexpensive and high-throughput procedure to extract and purify total genomic DNA for population studies. Mol Ecol Notes 3:317–320.

  18. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–20.

  19. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567.

  20. Fitzpatrick BM, Fordyce JA, Niemiller ML, Reynolds RG (2012) What can DNA tell us about biological invasions? Biol Invasions 14:245–253.

  21. Gherardi F, Gollasch S, Minchin D, Olenin S, Panov VE (2009) Alien invertebrates and fish in European inland waters. In: DAISIE (ed.) Handbook of Alien Species in Europe. Springer, Dordrecht, 81–92.

  22. Goudet J, Jombart T (2015) hierfstat: estimation and tests of hierarchical F-statistics. R package version 0.04-22.

  23. Grigorovich IA, Colautti RI, Mills EL, Holeck K, Ballert AG, MacIsaac HJ (2003) Ballast-mediated animal introductions in the Laurentian Great Lakes: retrospective and prospective analyses. Can J Fish Aquat Sci 60:740–756.

  24. Grosholz ED (1996) Contrasting rates of spread for introduced species in terrestrial and marine systems. Ecology 77:1680–1686.

  25. Hayden TA, Miner JG (2009) Rapid dispersal and establishment of a benthic Ponto-Caspian goby in Lake Erie: Diel vertical migration of early juvenile Round Goby. Biol Invasions 11:1767–1776.

  26. Hensler SR, Jude DJ (2007) Diel vertical migration of Round Goby larvae in the Great Lakes. J Gt Lakes Res 33:295–302.

  27. Hirsch PE, Adrian-Kalchhauser I, Flämig S, N’Guyen A, Defila R, Di Giulio A, Burkhardt-Holm P (2016a) A tough egg to crack: recreational boats as vectors for invasive goby eggs and transdisciplinary management approaches. Ecol Evol 6:707–715.

  28. Hirsch PE, N’Guyen A, Adrian-Kalchhauser I, Burkhardt-Holm P (2016b) What do we really know about the impacts of one of the 100 worst invaders in Europe? A reality check. Ambio 45:267–279.

  29. Horvitz N, Wang R, Wan F-H, Nathan R (2017) Pervasive human-mediated large-scale invasion: analysis of spread patterns and their underlying mechanisms in 17 of China’s worst invasive plants. J Ecol 105:85–94.

  30. Jude DJ (2000) Round and Tubenose Gobies: 10 years with the latest Great Lakes phantom menace. Dreissena! 11:1–13.

  31. Jude DJ (1997) Round Gobies: cyberfish of the third millenium. Gt Lakes Res Rev 3:27–34.

  32. Jude DJ, Janssen J, Crawford G (1995) Ecology, distribution, and impact of the newly introduced Round & Tubenose Gobies on the biota of the St. Clair & Detroit Rivers. In: Munawar M, Edsall T, Leach J (eds) The Lake Huron ecosystem: fisheries and management. SPB Academic Publishing, Amsterdam, Netherlands, p 447–460.

  33. Jude DJ, Reider RH, Smith GR (1992) Establishment of Gobiidae in the Great Lakes Basin. Can J Fish Aquat Sci 49:416–421.

  34. Kornis MS, Mercado-Silva N, vander Zanden MJ (2012) Twenty years of invasion: a review of Round Goby Neogobius melanostomus biology, spread and ecological implications. J Fish Biol 80:235–285.

  35. Kornis MS, Vander Zanden MJ (2010) Forecasting the distribution of the invasive Round Goby (Neogobius melanostomus) in Wisconsin tributaries to Lake Michigan. Can J Fish Aquat Sci 67:553–562.

  36. Kotta J, Nurkse K, Puntila R, Ojaveer H (2016) Shipping and natural environmental conditions determine the distribution of the invasive non-indigenous Round Goby Neogobius melanostomus in a regional sea. Estuar Coast Shelf Sci 169:15–24.

  37. LaRue EA, Ruetz CR, Stacey MB, Thum RA (2011) Population genetic structure of the Round Goby in Lake Michigan: implications for dispersal of invasive species. Hydrobiologia 663:71–82.

  38. Macinnis AJ, Corkum LD (2000) Fecundity and reproductive season of the Round Goby Neogobius melanostomus in the Upper Detroit River. Am Fish Soc 129:136–144.

  39. Marsden JE, Charlebois P, Wolfe K, Jude DJ, Rudnicka S (1996) The Round Goby, Neogobius melanostomus (Pallas): a review of European and North American literature. Illinois Natural History Survey, Zion, Illinois.

  40. Matthews J, Van der Velde G, Bij de Vaate A, Collas FPL, Koopman KR, Leuven RSEW (2014) Rapid range expansion of the invasive quagga mussel in relation to zebra mussel presence in The Netherlands and Western Europe. Biol Invasions 16:23–42.

  41. Mills EL, Leach JH, Carlton JT, Secor CL (1993) Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. J Gt Lakes Res 19:1–54.

  42. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538.

  43. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.

  44. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539.

  45. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–59.

  46. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

  47. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201.

  48. Ray WJ, Corkum LD (2001) Habitat and site affinity of the Round Goby. J Gt Lakes Res 27:329–334.

  49. Ricciardi A (2006) Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Divers Distrib 12:425–433.

  50. Ricciardi A (2007) Are modern biological invasions an unprecedented form of global change? Conserv Biol 21:329–336.

  51. Roche KF, Janač M, Jurajda P (2013) A review of Gobiid expansion along the Danube-Rhine corridor – geopolitical change as a driver for invasion. Knowl Manag Aquat Ecosyst 411:01.

  52. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228.

  53. Skora KE, Stolarski J (1993) New fish species in the Gulf of Gdansk, Neogobius spp. [cf. Neogobius melanostomus (Pallas 1811).]. Bull Sea Fish Inst 1:83–84.

  54. Snyder MR, Stepien CA (2017) Genetic patterns across an invasion’s history: a test of change versus stasis for the Eurasian Round Goby in North America. Mol Ecol 26:1075–1090.

  55. Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55:152–174.

  56. Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: Insights from Argentine ants. Proc Natl Acad Sci USA 98:1095–1100.

  57. U.S. Geological Survey (2017) Nonindigenous Aquatic Species Database.

  58. United States Coast Guard (1993) Ballast water management for vessels entering the Great Lakes. United States Coast Guard, Washington, DC.

  59. Wolfe KR, Marsden EJ (1998) Tagging methods for the round goby (Neogobius melanostomus). J Gt Lakes Res 24:731–735.

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The authors would like to thank R. Walter and K. McLean for valuable input on early versions of the manuscript. Funding was provided by NSERC Discovery grants to H.J.M. and D.D.H., and a Canada Research Chair to H.J.M. The manuscript was greatly improved by the suggestions of two anonymous reviewers.

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  1. Great Lakes Institute for Environmental Research, University of Windsor, 401 Sunset Ave., Windsor, ON, N9B 3P4, Canada

    • Mattias L. Johansson
    • , Bradley A. Dufour
    • , Kyle W. Wellband
    • , Lynda D. Corkum
    • , Hugh J. MacIsaac
    •  & Daniel D. Heath


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Correspondence to Mattias L. Johansson.

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