Invader invaded: population dynamics of zebra mussels (Dreissena polymorpha) and quagga mussels (Dreissena rostriformis bugensis) in polymictic Oneida Lake, NY, USA (1992–2013)

Abstract

Invasive zebra (ZM) and quagga (QM) mussels continue to spread within and across inland waters worldwide. Oneida Lake, NY, USA, is a large (207 km2), mesotrophic, polymictic lake surveyed annually for dreissenids across substrates since 1992. We estimated abundance and distribution of ZMs and QMs across substrates, calculated lakewide density and biomass, analyzed seasonal and annual differences in veliger density, and explored dynamics of species replacement. ZMs and QMs were detected in 1991 and 2005, respectively. ZM density peaked at almost 30,000 ind/m2 in 1992, declined to between 2600 and 7600 ind/m2 until 2008, and further declined to 370–560 ind/m2 in 2010–2013 concurrent with increasing QM abundance. ZM biomass remained stable from 1992 to 2008 (140–530 g shell-on dry wt/m2) but declined to < 10 g from 2010 to 2013. QMs increased from 38% of the total biomass in 2008 to ≥ 90% from 2010 to 2013 which was accompanied by a decrease in ZM lengths and increase in QM lengths. In shallow (< 9 m) waters, both mussels were more abundant on rock than sand and silt substrate. Only QMs were abundant in deep silt substrate. The shift from ZM to QM dominance increased total biomass, but not density, due to larger QMs. Veliger densities were higher in May and August–November after arrival of QMs; however, there was no correlation between number of veligers and new recruits in fall or adult mussel biomass. The replacement of ZM occurred over about 4 years even though published mechanisms for QM dominance are not operating in summer in Oneida Lake.

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References

  1. Baldwin BS, Mayer MS, Dayton J, Pau N, Mendilla J, Sullivan M et al (2002) Comparative growth and feeding in zebra and quagga mussels (Dreissena polymorpha and Dreissena bugensis): implications for North American lakes. Can J Fish Aquat Sci 59:680–694

    Article  Google Scholar 

  2. Barbiero RP, Lesht BM, Warren GJ, Rudstam LG, Watkins JM, Reavie ED et al (2018) A comparative examination of recent changes in nutrients and lower food web structure in Lake Michigan and Lake Huron. J Great Lakes Res 44:573–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Birkett K, Lozano S, Rudstam LG (2015) Long-term trends in Lake Ontario’s benthic macroinvertebrate community from 1994–2008. Aquat Ecosyst Health Manag 18:76–85

    Article  Google Scholar 

  4. Burlakova LE, Karatayev AY, Padilla DK (2006) Changes in the distribution and abundance of Dreissena polymorpha within lakes through time. Hydrobiologia 517:133–146

    Article  Google Scholar 

  5. Chu C, Minns CK, Moore JE, Millard ES (2004) Impact of oligotrophication, temperature, and water levels on walleye habitat in the Bay of Quinte, Lake Ontario. Trans Am Fish Soc 133:868–879

    Article  Google Scholar 

  6. Claxton WT, Mackie GL (1998) Seasonal and depth variations in gametogenesis and spawning of Dreissena polymorpha and Dreissena bugensis in eastern Lake Erie. Can J Zool 76:2010–2019

    Article  Google Scholar 

  7. Diggins TP (2001) A seasonal comparison of suspended sediment filtration by quagga (Dreissena bugensis) and zebra (D. polymorpha) mussels. J Great Lakes Res 27:457–466

    Article  Google Scholar 

  8. Fitzgerald D, Zhu B, Mills E, Rudstam L, Hoskins S, Haddad D et al (2016) Dynamics of aquatic vegetation in Oneida Lake, 1915–2005: a response to ecosystem changes. In: Rudstam L, Mills E, Jackson J, Stewart D (eds) Oneida Lake: long-term dynamics of a managed ecosystem and its fisheries. American Fisheries Society, Bethesda, pp 181–200

    Google Scholar 

  9. Ginn BK, Bolton R, Coulombe D, Fleischaker T, Yerex G (2018) Quantifying a shift in benthic dominance from zebra (Dreissena polymorpha) to quagga (Dreissena rostriformis bugensis) mussels in a large, inland lake. J Great Lakes Res 44:271–282

    Article  Google Scholar 

  10. Greeson P (1971) Limnology of Oneida Lake with emphasis on factors contributing to algae blooms. United States Department of the Interior Geological Survey, Albany

    Google Scholar 

  11. Hebert PDN, Muncaster BW, Mackie GL (1989) Ecological and genetic studies on Dreissena polymorpha (Pallas): a new mollusk in the Great Lakes. Can J Fish Aquat Sci 46:1587–1591

    Article  Google Scholar 

  12. Hetherington AL (2016) Ecological forecasting for Oneida Lake: impacts of climate change and invasive mussels on lake dynamics. Dissertation, Cornell University

  13. Higgins SN, Vander Zanden MJ (2010) What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecol Monogr 80:179–196

    Article  Google Scholar 

  14. Hunter RG, Simons KA (2004) Dreissenids in Lake St. Claire in 2001: evidence for population regulation. J Great Lakes Res 30:528–537

    Article  Google Scholar 

  15. Irwin BJ, Rudstam LG, Jackson JR, VanDeValk AJ, Forney JL, Fitzgerald DG (2009) Depensatory mortality, density-dependent growth, and delayed compensation: disentangling the interplay of mortality, growth, and density during early life stages of yellow perch. Trans Am Fish Soc 138:99–110

    Article  Google Scholar 

  16. Johnson LE (1995) Enhanced early detection and enumeration of zebra mussel (Dreissena spp.) veligers using cross-polarized light microscopy. Hydrobiologia 312:139–146

    Article  Google Scholar 

  17. Jones LA, Ricciardi A (2014) The influence of pre-settlement and early post-settlement processes on the adult distribution and relative dominance of two invasive mussel species. Freshw Biol 59:1086–1100

    Article  Google Scholar 

  18. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  19. Karatayev AY, Burlakova LE, Padilla DK (1997) The effects of Dreissena polymorpha (Pallas) invasion on aquatic communities in Eastern Europe. J Shellfish Res 16:187–203

    Google Scholar 

  20. Karatayev AY, Burlakova LE, Padilla DK (2002) Impacts of zebra mussels on aquatic communities and their role as ecosystem engineers. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe: distribution, impacts and management. Springer, Dordrecht, pp 433–446

    Google Scholar 

  21. Karatayev AY, Burlakova LE, Padilla DK (2006) Growth rate and longevity of Dreissena polymorpha (Pallas): a review and recommendation for future study. J Shellfish Res 25:23–32

    Article  Google Scholar 

  22. Karatayev AY, Burlakova LE, Mastitsky SE, Padilla DK, Mills EL (2011) Contrasting rates of spread of two congeners, Dreissena polymorpha and Dreissena rostriformis bugensis, at different spatial scales. J Shellfish Res 30:923–931

    Article  Google Scholar 

  23. Karatayev AY, Burlakova LE, Pennuto C, Ciborowski J, Karatayev VA, Juette P et al (2014) Twenty five years of change in Dreissena spp. populations in Lake Erie. J Great Lakes Res 40:550–559

    Article  Google Scholar 

  24. Karatayev AY, Burlakova LE, Padilla DK (2015) Zebra versus quagga mussels: a review of their spread, population dynamics, and ecosystem impacts. Hydrobiologia 746:97–112

    Article  CAS  Google Scholar 

  25. Kissman CEH, Knoll LB, Sarnelle O (2010) Dreissenid mussels (Dreissena polymorpha and Dreissena bugensis) reduce microzooplankton and macrozooplankton biomass in thermally stratified lakes. Limnol Oceanogr 55:1851–1859

    Article  Google Scholar 

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

    Article  Google Scholar 

  27. MacIsaac HJ, Sprules WG, Leach JH (1991) Ingestion of small-bodied zooplankton by zebra mussels: can cannibalism on larvae influence population dynamics? Can J Fish Aquat Sci 48:2151–2160

    Google Scholar 

  28. Marescaux J, Boets P, Lorquet J, Sablon R, Van Doninck K, Beisel J-N (2015) Sympatric Dreissena species in the Meuse River: towards a dominance shift from zebra to quagga mussels. Aquat Invasion 10:287–298

    Article  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. May B, Marsden JE (1992) Genetic identification and implications of another invasive species of dreissenid mussel in the Great Lakes. Can J Fish Aquat Sci 49:1501–1506

    Article  Google Scholar 

  31. Mayer CM, Rudstam LG, Mills EL, Cardiff SG, Bloom CA (2001) Zebra mussels (Dreissena polymorpha), habitat alteration, and yellow perch (Perca flavescens) foraging: system-wide effects and behavioural mechanisms. Can J Fish Aquat Sci 58:2459–2467

    Article  Google Scholar 

  32. Mayer CM, Keats RA, Rudstam LG, Mills EL (2002) Scale-dependent effects of zebra mussels on benthic invertebrates in a large eutrophic lake. J the N Am Benthol Soc 21:616–633

    Article  Google Scholar 

  33. Mayer CM, Burlakova LE, Eklöv P, Fitzgerald D, Karatayev AY, Ludsin SA et al (2014) Benthification of freshwater lakes: exotic mussels turning ecosystems upside down. In: Nalepa TF, Schloesser DW (eds) Quagga and zebra mussels: biology, impacts, and control, 2nd edn. CRC Press, Boca Raton, pp 575–585

    Google Scholar 

  34. Mayer CM, Zhu B, Cecala R (2016) The zebra mussel invasion of Oneida Lake: benthification of a eutrophic lake. In: Rudstam L, Mills E, Jackson J, Stewart D (eds) Oneida Lake: long-term dynamics of a managed ecosystem and its fisheries. American Fisheries Society, Bethesda, pp 161–180

    Google Scholar 

  35. Mei X, Zhang X, Kassam SS, Rudstam LG (2016) Will the displacement of zebra mussels by quagga mussels increase water clarity in shallow lakes during summer? Results from a mesocosm experiment. PLoS ONE 11:e0168494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Mellina E, Rasmussen JB, Mills EL (1995) Impact of the zebra mussel (Dreissena polymorpha) on phosphorus cycling and chlorophyll in lakes. Can J Fish Aquat Sci 52:2553–2573

    Article  CAS  Google Scholar 

  37. Miehls ALJ, Mason DM, Frank KA, Krause AE, Peacor SD, Taylor WW (2009) Invasive species impacts on ecosystem structure and function: a comparison of Oneida Lake, New York, USA, before and after zebra mussel invasion. Ecol Model 220:3194–3209

    Article  Google Scholar 

  38. Mills EL, Dermott RM, Roseman EF, Dustin D, Mellina E, Conn DB, Spidle AP (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 

  39. 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

    Article  Google Scholar 

  40. Mills EL, Chrisman JR, Baldwin B, Owens RW, O’Gorman R, Howell T et al (1999) Changes in the dreissenid community in the lower Great Lakes with emphasis on southern Lake Ontario. J Great Lakes Res 25:187–197

    Article  Google Scholar 

  41. Mills EL, Casselman JM, Dermott R, Fitzsimons JD, Gal G, Holeck KT et al (2003) Lake Ontario: food web dynamics in a changing ecosystem (1970–2000). Can J Fish Aquat Sci 60:471–490

    Article  Google Scholar 

  42. Mills E, Forney J, Holeck K (2016) Oneida Lake: A century of biotic introductions and ecosystem change. In: Rudstam L, Mills E, Jackson J, Stewart D (eds) Oneida Lake: long-term dynamics of a managed ecosystem and its fisheries. American Fisheries Society, Bethesda, pp 87–110

    Google Scholar 

  43. Naddafi R, Rudstam LG (2013) Predator-induced behavioural defences in two competitive invasive species. Anim Behav 86:1275–1284

    Article  Google Scholar 

  44. Naddafi R, Rudstam LG (2014a) Does differential predation explain the replacement of zebra by quagga mussels? Freshw Sci 33:895–903

    Article  Google Scholar 

  45. Naddafi R, Rudstam LG (2014b) Predator-induced morphological defences in two invasive dreissenid mussels: implications for species replacement. Freshw Biol 59:703–713

    Article  Google Scholar 

  46. Naddafi R, Blenckner P, Eklöv P, Pettersson K (2011) Physical and chemical properties determine zebra mussel invasion success in lakes. Hydrobiologia 669:227–236

    Article  CAS  Google Scholar 

  47. Nakano D, Strayer DL (2014) Biofouling animals in fresh water: biology, impacts, and ecosystem engineering. Front Ecol Environ 12:167–175

    Article  Google Scholar 

  48. Nalepa TF, Schloesser DW (eds) (2014) Quagga and zebra mussels: biology, impacts, and control, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  49. Nalepa TF, Wojcik JA, Fanslow DL, Lang GA (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 

  50. Nalepa TF, Fanslow DL, Lang GA (2009) Transformation of the offshore benthic community in Lake Michigan: recent shift from the native amphipod Diporeia spp. to the invasive mussel Dreissena rostriformis bugensis. Freshw Biol 54:466–479

    Article  Google Scholar 

  51. Nalepa TF, Fanslow DL, Pothoven SA (2010) Recent changes in density, biomass, recruitment, size structure, and nutritional state of Dreissena populations in southern Lake Michigan. J Great Lakes Res 36:5–19

    Article  CAS  Google Scholar 

  52. O’Neill CR Jr (1997) Economic impact of zebra mussels: results of the 1995 National Zebra Mussel Information Clearinghouse study. Great Lakes Res Rev 3:35–42

    Google Scholar 

  53. Orlova MI, Muirhead JR, Antonov PI, Shcherbina GK, Starobogatov YI, Biochino GI et al (2005) Range expansion of quagga mussels (Dreissena rostriformis bugensis) in the Volga River and Caspian Sea basin. Aquat Ecol 38:561–573

    Article  Google Scholar 

  54. Patterson MW, Ciborowski JJ, Barton DR (2005) The distribution and abundance of Dreissena species (Dreissenidae) in Lake Erie, 2002. J Great Lakes Res 31:223–237

    Article  Google Scholar 

  55. Ram JL, Karim AS, Banno F, Kashian DR (2012) Invading the invaders: reproductive and other mechanisms mediating the displacement of zebra mussels by quagga mussels. Invertebr Reprod Dev 56:21–32

    Article  Google Scholar 

  56. Ramcharan CW, Padilla DK, Dodson SI (1992) Models to predict potential occurrence and density of the zebra mussel, Dreissena polymorpha. Can J Fish Aquat Sci 49:2611–2620

    Article  Google Scholar 

  57. Ray WJ, Corkum LD (1997) Predation of zebra mussels by round gobies, Neogobius melanostomus. Environ Biol Fishes 50:267–273

    Article  Google Scholar 

  58. Roe SL, MacIsaac HJ (1997) Deepwater population structure and reproductive state of quagga mussels (Dreissena bugensis) in Lake Erie. Can J Fish Aquat Sci 54:2428–2433

    Article  Google Scholar 

  59. Rudstam LG (2017a) Lakewide zebra and quagga mussel summary, Oneida Lake, New York, 1992 to present. Web data on Knowledge Network for Biocomplexity. Original data set published in 2008. Updated in 2017. https://knb.ecoinformatics.org/view/kgordon.23.54. Accessed 15 Jan 2019

  60. Rudstam LG (2017b) Benthic invertebrates in Oneida Lake, New York, 1964–present. Web data on Knowledge Network for Biocomplexity. Original data published in 2008. Updated in 2017. https://knb.ecoinformatics.org/view/kgordon.4.65. Accessed 15 Jan 2019

  61. Rudstam LG, Jackson JR, Hetherington AL (2016a) Concluding remarks: Forecasting the future of Oneida Lake and its fishery in an era of climate change and biological invasions. In: Rudstam L, Mills E, Jackson J, Stewart D (eds) Oneida Lake: long-term dynamics of a managed ecosystem and its fisheries. American Fisheries Society, Bethesda, pp 525–540

    Google Scholar 

  62. Rudstam LG, Mills EL, Jackson JR, Stewart DJ (eds) (2016b) Oneida Lake: Long-term dynamics of a managed ecosystem and its fishery. American Fisheries Society, Bethesda

    Google Scholar 

  63. Schaner T (1990) Detection of zebra mussel veliger in plankton samples using sugar solution. In: Ontario Ministry of Natural Resources Lake Ontario Fisheries Unit (ed) Lake Ontario Fisheries Unit 1990 annual report, LOA 91.1.. Ontario Ministry of Natural Resources, Picton, pp 6.1–6.3

  64. Sprung M (1989) Field and laboratory observations of Dreissena polymorpha larvae: abundance, growth, mortality, and food demands. Arch Hydrobiol 115:537–561

    Google Scholar 

  65. Stanczykowska A, Lewandowski K (1993) Thirty years of Dreissena polymorpha ecology in Mazurian Lakes of northeastern Poland. In: Nalepa TF, Schloesser DW (eds) Zebra mussels: biology, impacts, and control. Lewis Publishers, Boca Raton, pp 3–33

    Google Scholar 

  66. Stewart TW, Haynes JM (1994) Benthic macroinvertebrate communities of Southwestern Lake Ontario following invasion of Dreissena. J Great Lakes Res 20:479–493

    Article  Google Scholar 

  67. 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 

  68. Strayer DL, Malcom HM (2006) Long-term demography of a zebra mussel (Dreissena polymorpha) population. Freshw Biol 51:117–130

    Article  Google Scholar 

  69. Strayer DL, Adamovich BV, Adrian R, Aldridge DC, Balogh CS, Burlakova LE et al (in review) Long-term population dynamics of zebra and quagga mussels (Dreissena polymorpha and D. rostriformis): a cross-system analysis. Ecosphere

  70. Strayer DL, Caraco NF, Cole JJ, Findlay S, Pace ML (1999) Transformation of freshwater ecosystems by bivalves—a case study of zebra mussels in the Hudson River. Bioscience 49:19–27

    Article  Google Scholar 

  71. Taylor WA (2015) Change-point analysis: a powerful new tool for detecting changes. http://www.variation.com/files/articles/changepoint.pdf. Accessed 27 Aug 2015

  72. Vanderploeg HA, Liebig JR, Nalepa TF, Fahnenstiel GL, Pothoven SA (2010) Dreissena and the disappearance of the spring phytoplankton bloom in Lake Michigan. J Great Lakes Res 36:50–59

    Article  Google Scholar 

  73. Wilson KA, Howell ET, Jackson DA (2006) Replacement of zebra mussels by quagga mussels in the Canadian nearshore of Lake Ontario: the importance of substrate, round goby abundance, and upwelling frequency. J Great Lakes Res 32:11–28

    Article  Google Scholar 

  74. Zhu B, Fitzgerald DG, Mayer CM, Rudstam LG, Mills EL (2006) Alteration of ecosystem function by zebra mussels in Oneida Lake: impacts on submerged macrophytes. Ecosystems 9:1017–1028

    Article  Google Scholar 

  75. Zhukova TV, Radchikova NP, Mikheyeva TM, Veres JK, Medvinsky AB, Lukyanova EV (2017) Long-term dynamics of suspended matter in Naroch Lakes: trend or intervention. Inland Water Biol 10:250–257

    Article  Google Scholar 

  76. Zhulidov AV, Nalepa TF, Kozhara AV, Zhulidov DA, Gurtovaya TY (2006) Recent trends in relative abundance of two dreissenid species, Dreissena polymorpha and Dreissena bugensis in the Lower Don River system, Russia. Arch Hydrobiol 165:209–220

    Article  Google Scholar 

  77. Zhulidov AV, Kozhara AV, Scherbina GH, Nalepa TF, Protasov A, Afanasiev SA et al (2010) Invasion history, distribution, and relative abundances of Dreissena bugensis in the Old World: a synthesis of data. Biol Invasions 12:1923–1940

    Article  Google Scholar 

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Acknowledgments

We thank Edward Mills for the inspiration to study mussel dynamics in Oneida Lake and for leading the annual surveys of mussels in Oneida Lake from 1992 through 2009. Many technicians and graduate students at the Cornell Biological Field Station contributed to these data sets, including Spencer Hall, Fred Henson, Catherine Hoffman, Michael Hoffman, Rachel Keats, Jana Lantry, Eric Pueschel, Travis Spier, Jonathan Swan, and Carrie Wafer. We also wish to thank Lyubov Burlakova, Cayelan Carey, Nasseer Idrisi, Alexander Karatayev, and Christine Mayer for discussions on mussel dynamics and Ladd Johnson and an anonymous reviewer for helpful comments on the manuscript. This research was supported by Cornell University, New York State Department of Environmental Conservation (NYSDEC) grant to JRJ and LGR, and United States Department of Agriculture (USDA) National Institute of Food and Agriculture (NIFA), Hatch Project 0226747 to LGR, RLS and JRJ. Additional support to ALH was provided by Cayelan Carey at Virginia Polytechnic Institute and State University through a National Science Foundation (NSF) Grant 1517823. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the NIFA, NSF, NYSDEC, or USDA.

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Hetherington, A.L., Rudstam, L.G., Schneider, R.L. et al. Invader invaded: population dynamics of zebra mussels (Dreissena polymorpha) and quagga mussels (Dreissena rostriformis bugensis) in polymictic Oneida Lake, NY, USA (1992–2013). Biol Invasions 21, 1529–1544 (2019). https://doi.org/10.1007/s10530-019-01914-0

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Keywords

  • Biomass
  • Depth
  • Invasive species
  • Substrate
  • Veligers