SpringerLink
Log in

Invasive species alter ontogenetic shifts in the trophic ecology of Lake Sturgeon (Acipenser fulvescens) in the Niagara River and Lake Ontario

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Species invasions can alter food web structure and change ecosystem-level functioning, but it is often unclear how these invasions may affect the life history of native species. The Lake Sturgeon (Acipenser fulvescens), a large long-lived native fish species in the Great Lakes, has increased in abundance in the lower Niagara River and nearby Lake Ontario during a period of invasive species-induced ecosystem change precipitated most recently by Dreissenid mussels (Driessena polymorpha and Driessena bugensis) and Round Goby (Neogobius melanostomus). Material taken from cross-sections of archived pectoral spines from Niagara River Lake Sturgeon captured in 1998–2000 and 2010–2012 were analyzed for stable isotopes across discrete growth zones to provide an ontogenetic assessment of diet, and diet analysis of Lake Sturgeon captured in 2014 was conducted to assess the contribution of invasive prey. Round Goby was the most important Lake Sturgeon prey item (86% by weight) in 2014, which corroborated results of δ15N and δ13C. Lake Sturgeon captured after the invasion of Round Goby exhibited ontogenetic changes in δ15N that differed from pre-Round Goby patterns, though this effect was weaker for δ13C. Values of δ15N from spine growth zones indicated non-linear increases in trophic position with age and increased rate of δ15N enrichment after the Round Goby invasion. We conclude that Round Goby establishment in western Lake Ontario changed the feeding ecology of Lake Sturgeon, which may have a positive effect on population growth for this native species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Balshine S, Verma A, Chant V, Theysmeyer T (2005) Competitive interactions between round gobies and logperch. J Great Lakes Res 31:68–77

    Google Scholar 

  • Barbiero RP, Tuchman ML (2004) Changes in the crustacean communities of Lakes Michigan, Huron, and Erie following the invasion of the predatory cladoceran Bythotrephes longimanus. Can J Fish Aquat Sci 61:2111–2125

    Google Scholar 

  • Barton DR, Johnson RA, Campbell L, Petruniak J, Patterson M (2005) Effects of round gobies (Neogobius melanostomus) on dreissenid mussels and other invertebrates in eastern Lake Erie, 2002–2004. J Great Lakes Res 31:252–261

    Google Scholar 

  • Biesinger Z, Gorsky D, Jacobs GR, Sweka JA, Webb MAH, Talbott M (2014) Population assessment of Lake Sturgeon in the lower Niagara River. In: New York State Department of Environmental Conservation 2013 Annual Report to the Great lakes Fishery Commission’s Lake Ontario Committee, Windsor, Ontario, 26–27 March 2014

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  Google Scholar 

  • Bowen SH (1996) Quantitative description of diet. In: Murphy BR, Willis DW (eds) Fisheries techniques, 2nd edn. American Fisheries Society, Bethesda, pp 513–532

    Google Scholar 

  • Bruch RM, Campana SE, Davis-Foust SL, Hansen MJ, Janssen J (2009) Lake sturgeon age validation using bomb radiocarbon and known-age fish. Trans Am Fish Soc 138:361–372

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Capps KA, Flecker AS (2013) Invasive aquarium fish transform ecosystem nutrient dynamics. Proc R Soc B Biol Sci 280:20131520

    Google Scholar 

  • Carlson D (1995) Lake Sturgeon waters and fisheries in New York State. J Great Lakes Res 21(1):35–41

    Google Scholar 

  • Chalupnicki MA, Dittman DE, Carlson DM (2011) Distribution of Lake Sturgeon in New York: 11 years of restoration management. Am Midl Nat 165:364–371

    Google Scholar 

  • Crane DP, Einhouse DW (2016) Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby. J Great Lakes Res 42(2):405–412

    Google Scholar 

  • DeVries RJ, Schramm HL (2015) Similarities and differences in 13C and 15N stable isotope ratios in two non-lethal tissue types from shovelnose sturgeon Scaphirhynchus platorynchus (Rafinesque, 1820). J Appl Ichthyol 31:474–478

    CAS  Google Scholar 

  • Dorcas ME, Willson JD, Reed RN, Snow RW, Rochford MR, Miller MA, Meshaka WE, Andreadis PT, Mazzotti FJ, Romagosa CM, Hart KM (2012) Severe mammal declines coincide with proliferation of invasive Burmese pythons in Everglades National Park. Proc Natl A Sci USA 109:2418–2422

    CAS  Google Scholar 

  • Ellis BK, Stanford JA, Goodman D, Stafford CP, Gustafson DL, Beauchamp DA, Chess DW, Craft JA, Deleray MA, Hansen BS (2011) Long-term effects of a trophic cascade in a large lake ecosystem. Proc Natl A Sci USA 108:1070–1075

    CAS  Google Scholar 

  • Estrada JA, Rice AN, Natanson LJ, Skomal GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87:829–834

    PubMed  Google Scholar 

  • Fry B (1991) Stable isotope diagrams of freshwater food webs. Ecology 72:2293–2297

    Google Scholar 

  • Haley N (1998) A gastric lavage technique for characterizing diets of sturgeons. N Am J Fish Manage 18:978–981

    Google Scholar 

  • He JX, Ebener MP, Riley SC, Cottrill A, Kowalski A, Koproski S, Mohr L, Johnson JE (2012) Lake Trout status in the main basin of Lake Huron, 1973–2010. N Am J Fish Manag 32:402–412

    Google Scholar 

  • Hecky RE, Smith RE, Barton DR, Guildford SJ, Taylor WD, Charlton MN, Howel T (2004) The nearshore phosphorus shunt: a consequence of ecosystem engineering by dreissenids in the Laurentian Great Lakes. Can J Fish Aquat Sci 61(7):1285–1293

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 1992:181–188

    Google Scholar 

  • Hughes TC, Lowie CE, Haynes JM (2005) Age, growth, relative abundance, and scuba capture of a new or recovering spawning population of lake sturgeon in the lower Niagara River, New York. N Am J Fish Manag 25:1263–1272

    Google Scholar 

  • Hutchings JA (1993) Adaptive life histories effected by age-specific survival and growth rate. Ecology 74(3):673–684

    Google Scholar 

  • Jackson JR, VanDeValk AJ, Brooking TE, VanKeeken OA, Rudstam LG (2002) Growth and feeding dynamics of lake sturgeon, Acipenser fulvescens, in Oneida Lake, New York: results from the first five years of a restoration program. J Appl Ichthyol 18:439–443

    Google Scholar 

  • Jacobs GR, Madenjian CP, Bunnell DB, Holuszko JD (2010) Diet of lake trout and burbot in northern Lake Michigan during spring: evidence of ecological interaction. J Great Lakes Res 36:312–317

    Google Scholar 

  • Janssen J, Jude DJ (2001) Recruitment failure of mottled sculpin Cottus bairdi in Calumet Harbor, Southern Lake Michigan, Induced by the newly introduced Round Goby Neogobius melanostomus. J Great Lakes Res 27:319–328

    Google Scholar 

  • Johnson TB, Bunnell DB, Knight CT (2005) A potential new energy pathway in central Lake Erie: the Round Goby connection. J Great Lakes Res 31:238–251

    Google Scholar 

  • Kelly MH, Hagar WG, Jardine TD, Cunjak RA (2006) Nonlethal sampling of sunfish and slimy sculpin for stable isotope analysis: how scale and fin tissue compare with muscle tissue. N Am J Fish Manag 26:921–925

    Google Scholar 

  • Kim SL, Tinker MT, Estes JA, Koch PL (2012) Ontogenetic and among-individual variation in foraging strategies of northeast pacific white sharks based on stable isotope analysis. PLoS ONE 7:e45068. doi:10.1371/journal.pone.0045068

    PubMed  PubMed Central  CAS  Google Scholar 

  • King RB, Ray JM, Stanford KM (2006) Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Can J Zool 84:108–115

    Google Scholar 

  • Krueger CC, Perkins DL, Mills EL, Marsden JE (1995) Predation by alewives on lake trout fry in Lake Ontario: role of an exotic species in preventing restoration of a native species. International conference on restoration of Lake Trout in the Laurentian Great Lakes 21, Supplement 1:458–469

  • Lugendo BR, Nagelkerken I, Van Der Velde G, Mgaya YD (2006) The importance of mangroves, mud and sand flats, and seagrass beds as feeding areas for juvenile fishes in Chwaka Bay, Zanzibar: gut content and stable isotope analyses. J Fish Biol 69(6):1639–1661

    CAS  Google Scholar 

  • Madenjian CP, O’Gorman R, Bunnell DB, Argyle RL, Roseman EF, Warner DM, Stockwell JD, Stapanian MA (2008) Adverse effects of alewives on Laurentian Great Lakes fish communities. N Am J Fish Manag 28:263–282

    Google Scholar 

  • Madenjian CP, Stapanian M, Witzel L, Einhouse D, Pothoven S, Whitford H (2011) Evidence for predatory control of the invasive Round Goby. Biol Invasions 13:987–1002

    Google Scholar 

  • Madenjian CP, Rutherford ES, Stow CA, Roseman EF, He JX (2013) Trophic Shift, Not Collapse. Environ Sci Technol 47:11915–11916

    PubMed  CAS  Google Scholar 

  • Mendes S, Newton J, Reid R, Zuur A, Pierce G (2007) Stable carbon and nitrogen isotope ratio profiling of sperm whale teeth reveals ontogenetic movements and trophic ecology. Oecologia 151:605–615

    PubMed  Google Scholar 

  • Miller MA, Holey ME (1992) Diets of Lake Trout inhabiting nearshore and offshore Lake Michigan environments. J Great Lakes Res 18:51–60

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • Nilo P, Tremblay S, Bolon A, Dodson J, Dumont P, Fortin R (2006) Feeding ecology of juvenile lake sturgeon in the St. Lawrence River System. Trans Am Fish Soc 135:1044–1055

    Google Scholar 

  • Olson MH (1996) Ontogenetic niche shifts in largemouth bass: variability and consequences for first-year growth. Ecology 77:179–190

    Google Scholar 

  • O'Gorman R, Elrod JH, Owens RW, Schneider CP, Eckert TH, Lantry BF (2000) Shifts in depth distributions of alewives, rainbow smelt, and age-2 lake trout in southern Lake Ontario following establishment of dreissenids. Trans Am Fish Soc 129(5):1096–1106

    Google Scholar 

  • Ozersky T, Evans DO, Barton DR (2012) Invasive mussels alter the littoral food web of a large lake: stable isotopes reveal drastic shifts in sources and flow of energy. PLoS ONE 7:e51249

    PubMed  PubMed Central  CAS  Google Scholar 

  • Paterson G, Rush SA, Arts MT, Drouillard KG, Haffner GD, Johnson TB, Lantry BF, Hebert CE, McGoldrick DJ, Backus SM, Fisk AT (2014) Ecological tracers reveal resource convergence among prey fish species in a large lake ecosystem. Freshw Biol 59:2150–2161

    CAS  Google Scholar 

  • Perga ME, Gerdeaux D (2003) Using the δ13C and δ15N of whitefish scales for retrospective ecological studies: changes in isotope signatures during the restoration of Lake Geneva, 1980–2001. J Fish Biol 63:1197–1207

    Google Scholar 

  • Peterson D, Vecsei P, Jennings C (2007) Ecology and biology of the Lake Sturgeon: a synthesis of current knowledge of a threatened North American Acipenseridae. Rev Fish Biol Fish 17:59–76. doi:10.1007/s11160-006-9018-6

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015) nlme: linear and nonlinear mixed effects models. R package version 3.1-119. http://CRAN.R-project.org/package=nlme

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Google Scholar 

  • Post DM (2003) Individual variation in the timing of ontogenetic niche shifts in largemouth bass. Ecology 84:1298–1310

    Google Scholar 

  • Pothoven SA, Madenjian CP (2008) Changes in consumption by alewives and lake whitefish after dreissenid mussel invasions in Lakes Michigan and Huron. N Am J Fish Manag 28:308–320

    Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Steinhart GB, Stein RA, Marschall EA (2004a) High growth rate of young-of-the-year smallmouth bass in Lake Erie: a result of the Round Goby invasion? J Great Lakes Res 30:381–389

    Google Scholar 

  • Steinhart GB, Marschall EA, Stein RA (2004b) Round Goby predation on smallmouth bass offspring in nests during simulated catch-and-release angling. Trans Am Fish Soc 133:121–131

    Google Scholar 

  • Thomas MV, Haas RC (2002) Abundance, age structure, and spatial distribution of lake sturgeon, Acipenser fulvescens, in the St Clair System. J Appl Ichthyol 18(4):495–501

    Google Scholar 

  • Turschak BA, Bootsma HA (2015) Lake Michigan trophic structure as revealed by stable C and N isotopes. J Great Lakes Res. doi:10.1016/j.jglr.2015.04.004

    Article  Google Scholar 

  • Turschak BA, Bunnell D, Czesny S, Höök TO, Janssen J, Warner D, Bootsma HA (2014) Nearshore energy subsidies support Lake Michigan fishes and invertebrates following major changes in food web structure. Ecology 95:1243–1252

    PubMed  Google Scholar 

  • Vander Zanden MJ, Casselman JM, Rasmussen JB (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464–467

    CAS  Google Scholar 

  • Vander Zanden MJ, Shuter BJ, Lester NP, Rasmussen JB (2000) Within-and among-population variation in the trophic position of a pelagic predator, lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 57(4):725–731

    Google Scholar 

  • Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708

    PubMed  Google Scholar 

  • Walsh MG, Dittman DE, O’Gorman R (2007) Occurrence and food habits of the Round Goby in the Profundal Zone of Southwestern Lake Ontario. J Great Lakes Res 33:83–92

    Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425

    Google Scholar 

Download references

Acknowledgements

This manuscript was much improved by the helpful comments provided by John Sweka, Mike Millard, and four anonymous reviewers. Brian Layton, Zy Biesinger, Zeb Woiak, Jonah Withers, and many others helped assist with fieldwork and sample processing. Mention of specific products does not constitute endorsement by the U.S. Government. This study was funded by the Great Lakes Restoration Initiative. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author information

Authors and Affiliations

  1. Northeast Fishery Center, U.S. Fish and Wildlife Service, Lamar, PA, 16848, USA

    Gregory R. Jacobs

  2. Great Lakes Center, Buffalo State College, Buffalo, NY, 14222, USA

    Eric L. Bruestle

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

    Anna Hussey & Aaron T. Fisk

  4. Lower Great Lakes Fish and Wildlife Conservation Office, U.S. Fish and Wildlife Service, Basom, NY, 14013, USA

    Eric L. Bruestle & Dimitry Gorsky

  5. Odum School of Ecology, University of Georgia, Athens, GA, 30601, USA

    Gregory R. Jacobs

Authors
  1. Gregory R. Jacobs
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eric L. Bruestle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anna Hussey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dimitry Gorsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aaron T. Fisk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregory R. Jacobs.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jacobs, G.R., Bruestle, E.L., Hussey, A. et al. Invasive species alter ontogenetic shifts in the trophic ecology of Lake Sturgeon (Acipenser fulvescens) in the Niagara River and Lake Ontario. Biol Invasions 19, 1533–1546 (2017). https://doi.org/10.1007/s10530-017-1376-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-017-1376-6

Keywords

Search

Navigation