Advertisement

Oecologia

, Volume 159, Issue 4, pp 789–802 | Cite as

Resource switching in fish following a major food web disruption

  • Michael D. Rennie
  • W. Gary Sprules
  • Timothy B. Johnson
Ecosystem Ecology - Original Paper

Abstract

Dreissenid mussels (Dreissena polymorpha and D. bugensis) have re-engineered Great Lakes ecosystems since their introduction in the late 1980s. Dreissenids can have major indirect impacts on profundal habitats by redirecting nutrients and energy away from pelagic production (which supplies profundal production) and depositing nutrients and energy in the nearshore zones that they occupy. However, strong empirical evidence for the effects of this redirection of resources on fish populations is currently lacking. Here, we report significant shifts in isotopic signatures, depth distribution and diets of a coldwater profundal fish population that are all consistent with a greater reliance on nearshore resources after the establishment of dreissenid mussels in South Bay, Lake Huron. Isotopic signatures of scales collected from 5-year-old lake whitefish (Coregonus clupeaformis) demonstrated remarkable stability over the 50-year period prior to the establishment of dreissenids (1947–1997) and a sudden and significant change in isotopic signatures (3‰ enrichment in δ13C and 1‰ depletion in δ15N) after their establishment (2001–2005). These dramatic shifts in isotopic signatures were accompanied by a coincident shift in the mean depth of capture of lake whitefish towards the nearshore. A comparison of previously unpublished pre-invasion diets of lake whitefish from South Bay with contemporary diets collected between 2002 and 2005 also indicate a greater reliance on nearshore prey after the invasion of dreissenid mussels. This study is the first to report changes in the carbon source available to lake whitefish associated with restructured benthic communities after the appearance of dreissenid mussels. Further, this study contributes to a growing body of work that demonstrates the ecological insights that can be gained through isotopic analysis of archived fish bony tissues in ecosystems that have experienced significant levels of disturbance.

Keywords

Nearshore phosphorous shunt Dreissenids Biological invasion Stable isotopes Lake whitefish 

Notes

Acknowledgments

Chesley West helped prepare lake whitefish tissues for isotopic analysis, and Randolph Fernandez and Michael Yuille sorted benthic invertebrate samples. Nina Jakobi and Bridget Dilauro sorted and identified stomach contents for contemporary whitefish samples. John Stinchcombe graciously provided access to his microbalance. Bill Mark, Mike Power, Jake Vander Zanden, Chelsey Lumb and Blake Matthews provided insights into sample preparation and study design. Tanya Kenesky and Andrew Nicholson helped prepare ESM S1. Dave Anderson provided advice on interpreting archived data codes. Luke Hillyer, Nina Jakobi and Rob Keetch and the past and present captain and crew of the Atygamayg provided field support. Thanks to Bryan Henderson for reviving the South Bay field program in 2001. Insightful comments from Bob Hecky improved the quality of the manuscript. This work was supported financially by grants from the Ontario Ministry of Natural Resources and the Canada Ontario Agreement to WGS, Natural Sciences and Engineering Research Council of Canada grants to MDR and WGS, a research grant from the Toronto Sportsmen’s Show and the Ontario Federation of Anglers and Hunters to MDR, Ontario Graduate Scholarships to MDR, and a Norman S. Baldwin Fishery Science Scholarship to MDR. The experiments performed here comply with the current laws of Canada.

Supplementary material

442_2008_1271_MOESM1_ESM.pdf (1024 kb)
Supplementary material 1 (PDF 1023 kb)
442_2008_1271_MOESM2_ESM.pdf (30 kb)
Supplementary material 2 (PDF 29 kb)
442_2008_1271_MOESM3_ESM.pdf (70 kb)
Supplementary material 3 (PDF 69 kb)

References

  1. Barbiero RP, Tuchman ML (2004) Long-term dreissenid impacts on water clarity in Lake Erie. J Gt Lakes Res 30:557–565Google Scholar
  2. Casselman JM, Collins JJ, Crossman EJ, Ihssen PE, Spangler GR (1981) Lake whitefish (Coregonus clupeaformis) stocks of the Ontario waters of Lake Huron. Can J Fish Aquat Sci 38:1772–1789CrossRefGoogle Scholar
  3. Cochran WG (1977) Sampling techniques. Wiley, New YorkGoogle Scholar
  4. Depew DC, Guildford SJ, Smith REH (2006) Nearshore-offshore comparison of chlorophyll a and phytoplankton production in the dreissenid-colonized eastern basin of Lake Erie. Can J Fish Aquat Sci 63:1115–1129CrossRefGoogle Scholar
  5. Dermott R (2001) Sudden disappearance of the amphipod Diporeia from Eastern Lake Ontario, 1993–1995. J Gt Lakes Res 27:423–433Google Scholar
  6. Dermott R, Kerec D (1997) Changes to the deepwater benthos of eastern Lake Erie since the invasion of Dreissena: 1979–1993. Can J Fish Aquat Sci 54:922–930CrossRefGoogle Scholar
  7. Edsall TA (1999) Preferred temperatures of juvenile lake whitefish. J Gt Lakes Res 25:583–588Google Scholar
  8. Fernandez RJ, Rennie, MD, Sprules, WG (In press) Changes in nearshore zooplankton associated with species invasions and potential effects on larval lake whitefish (Coregonus clupeaformis). Int Rev HydrobiolGoogle Scholar
  9. Forseth IN, Innis AF (2004) Kudzu (Pueraria montana): History, physiology, and ecology combine to make a major ecosystem threat. Crit Rev Plant Sci 23:401–413CrossRefGoogle Scholar
  10. Foster SE (2007) Co-occurrence and interactions of large invertebrate predators in relation to the Bythotrephes invasion. Ph.D. thesis, University of Toronto, TorontoGoogle Scholar
  11. France RL (1995) Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnol Oceanogr 40:1310–1313Google Scholar
  12. France RL (1998) Density-weighted δ13C analysis of detritivory and algivory in littoral macroinvertebrate communities of boreal headwater lakes. Ann Zool Fenn 35:187–193Google Scholar
  13. Gatz DF, Smith L (1995) The standard error of a weighted mean concentration. 1. Bootstrapping versus other methods. Atmos Environ 29:1185–1193CrossRefGoogle Scholar
  14. Gerdeaux D, Perga ME (2006) Changes in whitefish scales δ13C during eutrophication and reoligotrophication of subalpine lakes. Limnol Oceanogr 51:772–780Google Scholar
  15. Hart JL (1931) The food of the whitefish (Coregonus clupeaformis) in Ontario waters, with a note on the parasites. Contr Can Biol Fish 21:445–454Google Scholar
  16. Hecky RE, Hesslein RH (1995) Contributions of benthic algae to lake food webs as revealed by stable isotope analysis. J N Am Benthol Soc 14:631–653CrossRefGoogle Scholar
  17. Hecky RE, Smith REH, Barton DR, Guildford SJ, Taylor WD, Charlton MN, Howell T (2004) The nearshore phosphorus shunt: a consequence of ecosystem engineering by dreissenids in the Laurentian Great Lakes. Can J Fish Aquat Sci 61:1285–1293CrossRefGoogle Scholar
  18. Henderson BA, Fry FEJ (1987) Interspecific relations among fish species in South Bay, Lake Huron, 1949–84. Can J Fish Aquat Sci 44:10–14CrossRefGoogle Scholar
  19. Hobson KA (1990) Stable isotope analysis of marbled murrelets—evidence for fresh-water feeding and determination of trophic level. Condor 92:897–903CrossRefGoogle Scholar
  20. Hodell DA, Schelske CL (1998) Production, sedimentation, and isotopic composition of organic matter in Lake Ontario. Limnol Oceanogr 43:200–214Google Scholar
  21. Ihssen PE, Evans DO, Christie WJ, Reckahn JA, Desjardine RL (1981) Life-history, morphology, and electrophoretic characteristics of five allopatric stocks of lake whitefish (Coregonus clupeaformis) in the Great Lakes region. Can J Fish Aquat Sci 38:1790–1807CrossRefGoogle Scholar
  22. Jensen OP, Benson BJ, Magnuson JJ, Card VM, Futter MN, Soranno PA, Stewart KM (2007) Spatial analysis of ice phenology trends across the Laurentian Great Lakes region during a recent warming period. Limnol Oceanogr 52:2013–2026Google Scholar
  23. Jobling M (1981) Temperature tolerance and the final preferendum—rapid methods for the assessment of optimum growth temperatures. J Fish Biol 19:439–455CrossRefGoogle Scholar
  24. Johannsson OE, Dermott R, Graham DM, Dahl JA, Millard ES, Myles DD, LeBlanc J (2000) Benthic and pelagic secondary production in Lake Erie after the invasion of Dreissena spp. with implications for fish production. J Gt Lakes Res 26:31–54Google Scholar
  25. Kelly MH, Hagar WG, Jardine TD, Cunjak RA (2006) Non-lethal sampling of sunfish and slimy sculpin for stable isotope analysis: how scale and fin tissue compare with muscle tissue. North Am J Fish Manage 26:921–925CrossRefGoogle Scholar
  26. King JR, Shuter BJ, Zimmerman AP (1997) The response of the thermal stratification of South Bay (Lake Huron) to climatic variability. Can J Fish Aquat Sci 54:1873–1882CrossRefGoogle Scholar
  27. Kinnunen RE (2003) Great Lakes commercial fisheries. Michigan Sea Grant. http://www.miseagrant.umich.edu/fisheries/fish-commercial.html. Accessed 1-1-2008
  28. Lumb CE (2005) Comparison of lake whitefish (Coregonus clupeaformis) growth in Lake Erie and Lake Ontario. M.Sc. thesis, University of Windsor, WindsorGoogle Scholar
  29. Lumb CE, Johnson TB, Cook HA, Hoye JA (2007) Comparison of lake whitefish (Coregonus clupeaformis) growth, condition, and energy density between lakes Erie and Ontario. J Gt Lakes Res 33:314–325CrossRefGoogle Scholar
  30. McNickle GG, Rennie MD, Sprules WG (2006) Changes in benthic invertebrate communities of South Bay, Lake Huron following invasion by zebra mussels (Dreissena polymorpha), and potential effects on lake whitefish (Coregonus clupeaformis) diet and growth. J Gt Lakes Res 32:180–193CrossRefGoogle Scholar
  31. Mills KH, Chalanchuk SM (2004) The fin-ray method of aging lake whitefish. Ann Zool Fenn 41:215–223Google Scholar
  32. Mohr LC, Ebener MP (2005) Status of lake whitefish (Coregonus clupeaformis) in Lake Huron. In: Mohr LC, Nalepa TF (eds) Proceedings of a workshop on the dynamics of lake whitefish (Coregonus clupeaformis) and the amphipod Diporeia spp. in the Great Lakes. Great Lakes Fishery Commission Technical Report 66, pp 105–126Google Scholar
  33. Nalepa TF, Hartson DJ, Fanslow DL, Lang GA, Lozano SJ (1998) Declines in benthic macroinvertebrate populations in southern Lake Michigan, 1980–1993. Can J Fish Aquat Sci 55:2402–2413CrossRefGoogle Scholar
  34. Nalepa TF, Fanslow DL, Iii AJF, Lang GA, Eadie BJ, Quigley MA (2006) Continued disappearance of the benthic amphipod Diporeia spp. in Lake Michigan: is there evidence for food limitation? Can J Fish Aquat Sci 63:872–890CrossRefGoogle Scholar
  35. Nalepa TF, Fanslow DL, Pothoven SA, Foley AJ, Lang GA (2007) Long-term trends in benthic macroinvertebrate populations in Lake Huron over the past four decades. J Gt Lakes Res 33:421–436CrossRefGoogle Scholar
  36. Owens RW, Dittman DE (2003) Shifts in the diets of slimy sculpin (Cottus cognatus) and lake whitefish (Coregonus clupeaformis) in Lake Ontario following the collapse of the burrowing amphipod Diporeia. Aquat Ecosys Health Manage 6:311–323CrossRefGoogle Scholar
  37. 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 63:1197–1207CrossRefGoogle Scholar
  38. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  39. Pothoven SA, Madenjian CP (2008) Changes in consumption by alewives and lake whitefish after dreissenid mussel invasions in Lakes Michigan and Huron. North Am J Fish Manage 28:308–320CrossRefGoogle Scholar
  40. Pothoven SA, Nalepa TF, Schneeberger PJ, Brandt SB (2001) Changes in diet and body condition of lake whitefish in southern Lake Michigan associated with changes in benthos. North Am J Fish Manage 21:876–883CrossRefGoogle Scholar
  41. R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
  42. Reckahn JA (1970) Ecology of young lake whitefish (Coregonus clupeaformis) in South Bay, Manitoulin Island, Lake Huron. In: Lindsay CC, Woods CS (eds) The biology of coregonid fishes. University of Manitoba Press, Winnipeg, pp 437–460Google Scholar
  43. Sierszen ME, Peterson GS, Scharold JV (2006) Depth-specific patterns in benthic-planktonic food web relationships in Lake Superior. Can J Fish Aquat Sci 63:1496–1503CrossRefGoogle Scholar
  44. Sinnatamby RN, Bowman JE, Dempson JB, Power M (2007) An assessment of de-calcification procedures for δ13C and δ15N analysis of yellow perch, walleye and Atlantic salmon scales. J Fish Biol 70:1630–1635Google Scholar
  45. Smith BR, Tibbles JJ (1980) Sea lamprey (Petromyzon marinus) In lakes Huron, Michigan, and Superior - history of invasion and control, 1936–78. Can J Fish Aquat Sci 37:1780–1801CrossRefGoogle Scholar
  46. Suess HE (1955) Radiocarbon concentration in modern wood. Science 122:415–417CrossRefGoogle Scholar
  47. Syvaranta J, Vesala S, Rask M, Ruuhijarvi J, Jones RI (2008) Evaluating the utility of stable isotope analyses of archived freshwater sample materials. Hydrobiologia 600:121–130CrossRefGoogle Scholar
  48. Vander Zanden MJ, Rasmussen JB (1999) Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395–1404CrossRefGoogle Scholar
  49. Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066Google Scholar
  50. Verburg P (2007) The need to correct for the Suess effect in the application of δ13C in sediment of autotrophic Lake Tanganyika, as a productivity proxy in the Anthropocene. J Paleolimnol 37:591–602CrossRefGoogle Scholar
  51. Wang Q, An SQ, Ma ZJ, Zhao B, Chen JK, Li B (2006) Invasive Spartina alterniflora: biology, ecology and management. Acta Phytotaxon Sin 44:559–588CrossRefGoogle Scholar
  52. Zar JH (1999) Biostatistical analysis. Prentice Hall, TorontoGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Michael D. Rennie
    • 1
    • 2
  • W. Gary Sprules
    • 1
  • Timothy B. Johnson
    • 3
  1. 1.Aquatic Ecology GroupUniversity of Toronto at MississaugaMississaugaCanada
  2. 2.Environmental and Life Sciences ProgramTrent UniversityPeterboroughCanada
  3. 3.Ontario Ministry of Natural ResourcesPictonCanada

Personalised recommendations