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Low dissolved ions may limit secondary invasion of inland waters by exotic round gobies and dreissenid mussels in North America

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Abstract

Round gobies and dreissenid mussels, exotic species in the North American Great Lakes basin, are euryhaline organisms whose geographic spread and ecological impacts in freshwaters may be limited by low levels of dissolved ions such as calcium (Ca). We measured source populations of these exotics in the St. Lawrence River and found population densities of dreissenids (range of ~1,000–6,400 individuals m−2) and round gobies (6–32 individuals m−2) similar to those in other Great Lake locations from which they have spread inland. However, we found little evidence for their secondary invasion of inland tributary rivers and lakes of northern New York State. Using natural waters collected from inland ecosystems, we ran laboratory bioassays of reproduction, growth, and survival of several life stages of zebra and quagga mussels as well as the round goby. We found little difference in the responses of zebra and quagga mussels, with each species showing moderate reproductive success, growth, and survival at Ca concentrations > 13 mg L−1 and dramatic improvements at >18 mg L−1. Round gobies showed moderate survival in waters with Ca concentrations > 8 mg L−1 and high survival > 18 mg L−1. These bioassays are the first such experiments for quagga mussels and round gobies and show how all three species may be similarly restricted in their ability to invade and permanently colonize significant geographic regions of New York State and perhaps the US.

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References

  • Ackerman JD, Sim B, Nichols SJ, Claudi R (1994) A review of the early life history of zebra mussels (Dreissena polymorpha): comparisons with marine bivalves. Can J Zool 72:1169–1179

    Article  Google Scholar 

  • Allen YC, Ramcharan CW (2001) Dreissena distribution in commercial waterways of the US: using failed invasions to identify limiting factors. Can J Fish Aquat Sci 58:898–907

    Article  Google Scholar 

  • Bain MB (1999) Interpreting chemical data. In: Bain MB, Stevenson NJ (eds) Aquatic habitat assessment: common methods. American Fisheries Society, Bethesda, pp 181–192

    Google Scholar 

  • Baldwin BS, Newell RIE (1995) Feeding rate responses of oyster larvae (Crassostrea virginica) to seston quantity and composition. J Exp Mar Biol Ecol 189:77–91

    Article  Google Scholar 

  • Baldwin BS, Black M, Sanjur O, Gustafson R, Lutz RA, Vrijenhoek RC (1996) A diagnostic molecular marker for zebra mussels (Dreissena polymorpha) and potentially co-occurring bivalves: mitochondrial COI. Mol Mar Biol Biotechnol 5:9–14

    PubMed  CAS  Google Scholar 

  • Baldwin BS, Mayer M, Dayton J, Pau N, Moore A, Mendill J, Sullivan M, Ma AMT, Mills E (2002) Comparative growth and feeding in zebra and quagga mussels: implications for North American lakes. Can J Fish Aquat Sci 59:680–694

    Article  Google Scholar 

  • Barreto RE, Volpato GL (2004) Caution for using ventilatory frequency as an indicator of stress in fish. Behav Process 66:43–51

    Article  Google Scholar 

  • Bode RW, Novak MA, Abele LE, Heitzman DL, Smith AJ (2002) Quality assurance work plan for biological stream monitoring in New York State. Stream Biomonitoring Unit, Division of Water, NYS Dept. of Environmental Conservation. Albany, 54 pp

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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Casper AF, Johnson LE (2010) Contrasting shell/tissue characteristics of Dreissena polymorpha and Dreissena bugensis in relation to environmental heterogeneity in the St. Lawrence River. J Great Lakes Res 36:184–189

    Article  Google Scholar 

  • Charlebois PM, Marsden JE, Goettel RG, Wolfe RK, Jude DJ, Rudnika S (1997) The round goby, Neogobius melanostomus (Pallas), a review of European and North American literature. Ill Nat Hist Surv Special Publ 20:1–76

    Google Scholar 

  • Chase ME, Bailey RC (1999) The ecology of the zebra mussel (Dreissena polymorpha) in the lower Great Lakes of North America: I. Population dynamics and growth. J Great Lakes Res 25:107–121

    Article  Google Scholar 

  • Chiarenzelli J, Bregani A, Cady C, Whitney B, Lock R (2011) Variation in multi-element chemistry related to bedrock buffering: an example from the Adirondack region of northern New York, USA. Environ Earth Sci (in press)

  • Chotkowski MA, Ellen Marsden J (1999) Round goby and mottled sculpin predation on lake trout eggs and fry: field predictions from laboratory experiments. J Great Lakes Res 25:26–35

    Article  Google Scholar 

  • Claxton WT, Wilson AB, Mackie GL, Boulding EG (1998) A genetic and morphological comparison of shallow- and deep-water populations of the introduced dreissenid bivalve Dreissena bugensis. Can J Zool 76:1269–1276

    Google Scholar 

  • Cohen AN, Weinstein A (2001) Zebra mussel’s calcium threshold and implications for its potential distribution in North America. San Francisco Estuary Institute, Richmond. http://www.sfei.org/bioinvasions/Reports/2001-Zebramusselcalcium356.pdf. Accessed 5 Apr 2011

  • Cooke GD, Welch EB, Peterson SA, Newroth PR (1993) Restoration and management of lakes and reservoirs, 2nd edn. Lewis Publishers, Boca Raton

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Dennis TE, MacAvoy SE, Steg MB, Bulger AJ (1995) The association of water chemistry variables and fish condition in streams of Shenandoah National Park (USA). Water Air Soil Pollut 85:365–370

    Article  CAS  Google Scholar 

  • Dermott R, Bonnell R, Carou S, Dow J, Jarvis P (2003) Spatial distribution and population structure of the mussels Dreissena polymorpha and Dreissena bugensis in the Bay of Quinte, Lake Ontario, 1998 and 2000. Can Tech Rep Fish Aquat Sci 2479:58

    Google Scholar 

  • Drake JM, Bossenbroek JM (2004) The potential distribution of zebra mussels in the United States. Bioscience 54:931–941

    Article  Google Scholar 

  • Drake JM, Bossenbroek JM (2009) Profiling ecosystem vulnerability to invasion by zebra mussels with support vector machines. Theor Ecol 2:189–198

    Article  Google Scholar 

  • Ellis S, MacIsaac HJ (2009) Salinity tolerance of Great Lakes invaders. Freshw Biol 54:77–89

    Article  CAS  Google Scholar 

  • Farrell JM, Holeck K, Mills E, Hoffman C, Patil V (2010) Recent ecological trends in lower trophic levels of the international section of the St. Lawrence River: a comparison of the 1970s to the 2000s. Hydrobiologia 647:21–33

    Article  CAS  Google Scholar 

  • French JRP, Black MG (2009) Maximum length and age of round gobies (Apollonia melanostomus) in Lake Huron. J Freshw Ecol 24:173–175

    Article  Google Scholar 

  • Frischer ME, McGrath BR, Hansen AS, Vescio PA, Wyllie JA, Wimbush J, Nierzwicki-Bauer S (2005) Introduction pathways, differential survival of adult and larval zebra mussels (Dreissena polymorpha), and possible management strategies, in an Adirondack lake, Lake George, NY. Lake Reserv Manage 21:391–402

    Article  Google Scholar 

  • Harper L (2006) Surveys of the Grasse River and Wilson Hill Wildlife Management Area for the Presence of Non-Native Dreissenid Mussels. Final Report for the St. Lawrence-FDR Power Project, New York Power Authority, New York, 22 pp

  • Haynes JM, Tisch NA, Mayer CM, Rhyne RS (2005) Benthic macroinvertebrate communities in southwestern Lake Ontario following invasion of Dreissena and Echinogammarus: 1983 to 2000. J North Am Benthol Soc 24:148–167

    Article  Google Scholar 

  • Hickey B, Fowlie A (2005) First occurrence of the round goby, Neogobius melanostomus, in the St. Lawrence River at Cornwall, Ontario. Can Field Nat 119:582–583

    Google Scholar 

  • Hincks SS, Mackie GL (1997) Effects of pH, calcium, alkalinity, hardness, and chlorophyll on the survival, growth, and reproductive success of zebra mussels (Dreissena polymorpha) in Ontario lakes. Can J Fish Aquat Sci 54:2049–2057

    Article  CAS  Google Scholar 

  • Irons KS, McClelland MA, Pegg MA (2006) Expansion of round goby in the Illinois Waterway. Am Midl Nat 156:198–200

    Article  Google Scholar 

  • Johnson TB, Allen M, Corkum LD, Lee VA (2005) Comparison of Methods Needed to Estimate Population Size of Round Gobies (Neogobius melanostomus) in Western Lake Erie. J Great Lakes Res 31:78–86

    Article  Google Scholar 

  • Jones L, Ricciardi A (2005) Influence of physicochemical factors on the distribution and biomass of invasive mussels (Dreissena polymorpha and Dreissena bugensis) in the St. Lawrence River. Can J Fish Aquat Sci 62:1953–1962

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Karatayev AY, Burlakova LE, Padilla DK (1998) Physical factors that limit the distribution and abundance of Dreissena polymorpha (Pall.). J Shellfish Res 17:1219–1235

    Google Scholar 

  • Karatayev AY, Boltovskoy D, Padilla DK, Burlakova LE (2007) The invasive bivalves Dreissena polymorpha and Limnoperna fortunei: parallels, contrasts, potential spread and invasion impacts. J Shellfish Res 26:205–213

    Article  Google Scholar 

  • Kilgour BW, Mackie GL, Baker MA, Keppel R (1994) Effects of salinity on the condition and survival of zebra mussels (Dreissena polymorpha). Estuaries 17:385–393

    Article  Google Scholar 

  • Klauda RJ, Palmer RE, Lenkevich MJ (1987) Sensitivity of early life stages of blueback herring to moderate acidity and aluminium in soft freshwater. Estuaries 10:44–53

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Koutnik MA, Padilla DK (1994) Predicting the spatial distribution of Dreissena polymorpha (zebra mussel) among inland lakes of Wisconsin: modeling with a GIS. Can J Fish Aquat Sci 51:1189–1196

    Article  Google Scholar 

  • Kraft CE, Johnson LE (2000) Regional differences in rates and patterns of North America inland lake invasions by zebra mussels (Dreissena polymorpha). Can J Fish Aquat Sci 57:993–1001

    Article  Google Scholar 

  • Krakowiak PJ, Pennuto CM (2008) Fish and macroinvertebrate communities in tributary streams of eastern Lake Erie with and without round gobies (Neogobius melanostomus, Pallas 1814). J Great Lakes Res 34:675–689

    Google Scholar 

  • Lederer A, Massart J, Janssen J (2006) Impact of round gobies (Neogobius melanostomus) on Dreissenids (Dreissena polymorpha and Dreissena bugensis) and the Associated Macroinvertebrate Community Across an Invasion Front. J Great Lakes Res 32:1–10

    Article  Google Scholar 

  • Lozano SJ, Scharold JV, Nalepa TF (2001) Recent declines in benthic macroinvertebrate densities in Lake Ontario. Can J Fish Aquat Sci 58:518–529

    Article  Google Scholar 

  • Ludyanskiy ML, McDonald D, MacNeill D (1993) Impact of the zebra mussel, a bivalve invader. Dreissena polymorpha is rapidly colonizing hard surfaces throughout waterways of the United States and Canada. Bioscience 43:533–544

    Article  Google Scholar 

  • MacInnis A, Corkum LD (2000) Age and growth of round goby Neogobius melanostomus in the Upper Detroit River. Trans Am Fish Soc 129:852–858

    Article  Google Scholar 

  • Marmorek DR, Lacroix GL, Korman J, Parnell I, Watt WD (1998) Assessing the impacts of acidification on Atlantic salmon (Salmo salar): a simple model of stream chemistry. Can J Fish Aquat Sci 55:2117–2126

    Article  CAS  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 

  • Mellina E, Rasmussen J (1994) Patterns in the distribution and abundance of zebra mussel (Dreissena polymorpha) in rivers and lakes in relation to substrate and other physiochemical factors. Can J Fish Aquat Sci 51:1024–1036

    Article  Google Scholar 

  • Miller S, Haynes JM (1997) Factors limiting colonization of western New York creeks by the zebra mussel (Dreissena polymorpha). J Freshw Ecol 12:81–88

    Article  CAS  Google Scholar 

  • Mills E, Dermott R, Roseman E, Dustin D, Mellina E, Conn D, Spidle A (1993) Colonization, ecology, and population structure of the “quagga” mussel (Bivalvia: Dreissenidae) in the lower Great Lakes. Can J Fish Aquat Sci 50:2305–2314

    Article  Google Scholar 

  • Mills EL, Rosenberg G, Spidle AP, Ludyanskiy M, Pligin Y, May B (1996) A review of the biology and ecology of the quagga mussel (Dreissena bugensis), a second species of freshwater dreissenid introduced to North America. Am Zool 36:271–286

    Google Scholar 

  • Mills EL, Chrisman J, Baldwin B, Owens R, O’ Gorman R, Howell T, Roseman E, Raths M (1999) Changes in dreissenid community in the Lower Great Lakes with emphasis on southern Lake Ontario. J Great Lakes Res 25:187–197

    Article  Google Scholar 

  • Moskal’kova KI (1996) Ecological and morphophysiological prerequisites to range extension in the round goby Neogobius melanostomus under conditions of anthropogenic pollution. J Ichthyol 36:584–590

    Google Scholar 

  • Nalepa T, Wojcik J, Fanslow D, Lang G (1995) Initial colonization of the zebra mussel (Dreissena polymorpha) in Saginaw Bay, Lake Huron: population recruitment, density, and size structure. J Great Lakes Res 21:417–434

    Article  Google Scholar 

  • Neary B, Leach J (1992) Mapping the potential spread of the zebra mussel (Dreissena polymorpha) in Ontario. Can J Fish Aquat Sci 49:406–415

    Article  Google Scholar 

  • Ojaveer H (2006) The round goby Neogobius melanostomus is colonising the NE Baltic Sea. Aquat Invasions 1:44–45

    Article  Google Scholar 

  • Phillips EC, Washek ME, Hertel AW, Niebel BM (2003) The round goby (Neogobius melanostomus) in Pennsylvania tributary streams of Lake Erie. J Great Lakes Res 29:34–40

    Article  Google Scholar 

  • Poos M, Dextrase AJ, Schwalb AN, Ackerman JD (2010) Secondary invasion of the round goby into high diversity Great Lakes tributaries and species at risk hotspots: potential new concerns for endangered freshwater species. Biol Invasions 12:1269–1284

    Article  Google Scholar 

  • Ramcharan CW, Padilla DK, Dodson SI (1992) A multivariate model for predicting population fluctuations of Dreissena polymorpha in North American lakes. Can J Fish Aquat Sci 49:150–158

    Article  Google Scholar 

  • Ray WJ, Corkum LD (2001) Habitat and Site Affinity of the Round Goby. J Great Lakes Res 27:329–334

    Article  Google Scholar 

  • Reid D, Orlova M (2002) Geological and evolutionary underpinnings for the success of Ponto-Caspian species invasions in the Baltic Sea and North American Great Lakes. Can J Fish Aquat Sci 59:1144–1158

    Article  Google Scholar 

  • Ricciardi A, MacIsaac HJ (2000) Recent mass invasion of the North American Great Lakes by Ponto–Caspian species. Trends Ecol Evol 15:62–65

    Article  PubMed  Google Scholar 

  • Schaner T, Fox MG, Taraborelli AC (2009) An inexpensive system for underwater video surveys of demersal fishes. J Great Lakes Res 35:317–319

    Article  Google Scholar 

  • Schneider DW, Ellis C, Cummings K (1998) A transportation model assessment of the risk to native mussel communities from zebra mussel spread. Conserv Biol 12:788–800

    Article  Google Scholar 

  • Setzler-Hamilton EM, Wright DA, Magee JA (1997) Growth and spawning of laboratory-reared zebra mussels in lower mesohaline salinities. In: D’Itri FM (ed) Zebra mussels and aquatic nuisance species. Lewis Publishers/CRC Press, Boca Raton, pp 141–154

    Google Scholar 

  • Sinnich T, Mendenhall W (2003) A second course in statistics: regression analysis, 6th edn. Pearson Education, Upper Saddle River

    Google Scholar 

  • Sprung M (1987) Ecological requirements of developing Dreissena polymorpha eggs. Archiv fuer Hydrobiologie Supplement 79:69–86

    Google Scholar 

  • Stoeckmann A (2003) Physiological energetics of Lake Erie dreissenid mussels: a basis for the displacement of Dreissena polymorpha by Dreissena bugensis. Can J Fish Aquat Sci 60:126–134

    Article  Google Scholar 

  • Taraborelli AC, Fox MG, Schaner T, Johnson TB (2009) Density and habitat use by the round goby (Apollonia melanostoma) in the Bay of Quinte, Lake Ontario. J Great Lakes Res 35:266–271

    Article  Google Scholar 

  • USEPA (1987) Handbook of methods for acid deposition studies: laboratory analysis for surface water chemistry. EPA 600/4–87-026. Office of Science and Technology and Office of Water, Washington

    Google Scholar 

  • USEPA (1991) Data user’s guide to the US Environmental Protection Agency’s long-term monitoring project: quality assurance plan and data dictionary. EPA600/3e91/072. Office of Science and Technology and Office of Water, Washington, DC

    Google Scholar 

  • USEPA (2011) Great Lakes environmental database, United States Environmental Protection Agency. http://www.epa.gov/glnpo/monitoring/data_proj/glenda/glenda_query_index.html. Accessed 12 Mar 2011

  • USGS (2011a) Zebra and quagga mussel sightings distribution. United States Geological Survey. http://nas.er.usgs.gov/taxgroup/mollusks/zebramussel/maps/current_zm_quag_map.jpg. Accessed 21 Apr 2011

  • USGS (2011b) Round goby sightings distribution. United States Geological Survey. http://nas2.er.usgs.gov/viewer/omap.aspx?SpeciesID=713 Accessed 21 Apr 2011

  • USGS (2011c) Generate a nonindigenous species list. United States Geological Survey. http://nas.er.usgs.gov/queries/SpSearch.aspx Accessed 21 Apr 2011

  • Vinogradov GA, Smirnova NF, Sokolov VA, Bruznitsky AA (1993) Influence of chemical composition of the water on the mollusk Dreissena polymorpha. In: Nalepa TF, Schloesser DW (eds) Zebra mussels: biology, impacts, and control. Lewis Publishers/CRC Press, Boca Raton, pp 283–293

    Google Scholar 

  • Warren DR, Mineau MM, Ward EJ, Kraft CE (2010) Relating fish biomass to habitat and chemistry in headwater streams of the northeastern United States. Environ Biol Fishes 88:51–62

    Article  Google Scholar 

  • Whittier TR, Ringold P, Herlihy A, Pierson S (2008) A calcium-based invasion risk assessment for zebra and quagga mussels (Dreissena spp). Frontiers Ecol Environ 6:180–190

    Article  Google Scholar 

  • Wright DA, Setzler-Hamilton EM, Magee JA, Kennedy VS, McIninch SP (1996) Effect of salinity and temperature on survival and development of young zebra (Dreissena polymorpha) and quagga (Dreissena bugensis) mussels. Estuaries 19(3):619–628

    Article  Google Scholar 

  • Zhulidov A, Pavlov D, Nalepa TF, Scherbina G, Zhulidov D, Gurtovaya T (2004) Relative distributions of Dreissena bugensis and Dreissena polymorpha in the lower Don River system, Russia. Int Rev Hydrobiol 89:326–333

    Article  Google Scholar 

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Acknowledgments

We thank Dr. Michael Schuckers for help with statistical analyses, Carol Cady for help preparing Fig. 1, and Doug Brown, John Ashley, Adam Caswell and Jim Yaeger for assistance with scuba surveys. We are also grateful for access to data on surface water chemistry, shared by Dr. Scott Kisbaugh (NYSDEC Division of Water) and Dr. James McKenna (USGS Great Lakes Science Center). We also thank M. Kornis and an anonymous reviewer for their helpful comments on an earlier version of this paper. This research was supported by an A. C. Walker Foundation North Country Research Fellowship, a grant from the St. Lawrence River Research and Education fund, and additional financial assistance from St. Lawrence University. The US Environmental Protection Agency did not fund or manage the research described here. It has not been subject to Agency review and therefore does not necessarily reflect the views of the Agency. No official endorsement should be inferred.

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  1. Department of Biology, St. Lawrence University, Johnson Hall 123, Canton, NY, 13617, USA

    Brad S. Baldwin & Matthew Carpenter

  2. Health Effects Division, Environmental Protection Agency, Washington, DC, 20460, USA

    Kristin Rury

  3. Rodeph Sholom School, New York, NY, 10024, USA

    Erin Woodward

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  1. Brad S. Baldwin
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Correspondence to Brad S. Baldwin.

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Baldwin, B.S., Carpenter, M., Rury, K. et al. Low dissolved ions may limit secondary invasion of inland waters by exotic round gobies and dreissenid mussels in North America. Biol Invasions 14, 1157–1175 (2012). https://doi.org/10.1007/s10530-011-0146-0

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