Biological Invasions

, 13:2621 | Cite as

Bythotrephes invasion elevates trophic position of zooplankton and fish: implications for contaminant biomagnification

  • Michael D. RennieEmail author
  • Angela L. Strecker
  • Michelle E. Palmer
Original Paper


We estimated the effects of Bythotrephes longimanus invasion on the trophic position (TP) of zooplankton communities and lake herring, Coregonus artedi. Temporal changes in lacustrine zooplankton communities following Bythotrephes invasion were contrasted with non-invaded reference lakes, and along with published information on zooplankton and herring diets, formed the basis of estimated changes in TP. The TP of zooplankton communities and lake herring increased significantly following the invasion of Bythotrephes, whereas TP in reference lakes decreased (zooplankton) or did not change significantly (lake herring) over a similar time frame. Elevated TP following Bythotrephes invasion was most prominent in lakes that also supported the glacial relict, Mysis diluvania, suggesting a possible synergistic interaction between these two species on zooplankton community composition. Our analysis indicated that elevated TPs of zooplankton communities and lake herring are not simply due to the presence of Bythotrephes, but rather reflect changes in the zooplankton community induced by Bythotrephes; namely, a major reduction in the proportion of herbivorous cladoceran biomass and a concomitant increase in the proportion of omnivorous and/or predatory copepod biomass in invaded lakes. We demonstrated that increases in TP of the magnitude reported here can lead to substantial increases in fish contaminant concentrations. In light of these results, we discuss potential mechanisms that may be responsible for the disconnect between empirical and theoretical evidence that mid-trophic level species invasions (e.g., Bythotrephes) elevate contaminant burdens of consumer species, and provide testable hypotheses to evaluate these mechanisms.


Cercopagidae Mysis Fish Food web Contaminants Coregonidae 



We thank Bill Taylor for providing zooplankton biomass estimates from Jane Almond’s thesis. Jake La Rose and the Lake Simcoe Fisheries Assessment Unit (Ontario Ministry of Natural Resources) provided herring collections and funding for Hg and isotope determinations. Thanks also to Norm Yan for early discussions around this work and for organizing the workshops that ultimately led to this study, Bill Keller for providing access to the historical zooplankton data and Shelley Arnott for financial support and guidance. Scott Peacor and two anonymous reviewers provided helpful and constructive feedback on earlier drafts that improved the manuscript. This work was supported in part by Natural Sciences and Engineering Research Council of Canada (NSERC) Graduate scholarships to MDR, ALS and MEP, and by Ontario Graduate and York University graduate scholarships to MEP.

Supplementary material

10530_2011_81_MOESM1_ESM.pdf (153 kb)
Supplementary material 1 (PDF 154 kb)
10530_2011_81_MOESM2_ESM.pdf (95 kb)
Supplementary material 2 (PDF 95 kb)


  1. Adams SM, Kimmel BL, Ploskey GR (1983) Sources of organic-matter for reservoir fish production: a trophic-dynamics analysis. Can J Fish Aquat Sci 40:1480–1495CrossRefGoogle Scholar
  2. Almond MJR, Bentzen E, Taylor WD (1996) Size structure and species composition of plankton communities in deep Ontario lakes with and without Mysis relicta and planktivorous fish. Can J Fish Aquat Sci 53:315–325CrossRefGoogle Scholar
  3. Audzijonyte A, Väinölä R (2005) Diversity and distributions of circumpolar fresh- and brackish-water Mysis (Crustacea : Mysida): descriptions of M. relicta Loven, 1862, M. salemaai n. sp., M. segerstralei n. sp and M. diluviana n. sp., based on molecular and morphological characters. Hydrobiologia 544:89–141CrossRefGoogle Scholar
  4. 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 61:2111–2125CrossRefGoogle Scholar
  5. Boudreau SA, Yan ND (2003) The differing crustacean zooplankton communities of Canadian Shield lakes with and without the nonindigenous zooplanktivore Bythotrephes longimanus. Can J Fish Aquat Sci 60:1307–1313CrossRefGoogle Scholar
  6. Cabana G, Rasmussen JB (1994) Modeling food-chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature 372:255–257CrossRefGoogle Scholar
  7. Cabana G, Tremblay A, Kalff J, Rasmussen JB (1994) Pelagic food-chain structure in Ontario lakes: a determinant of mercury levels in lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 51:381–389CrossRefGoogle Scholar
  8. Campbell LM, Thacker R, Barton D, Muir DCG, Greenwood D, Hecky RE (2009) Re-engineering the eastern Lake Erie littoral food web: the trophic function of non-indigenous Ponto-Caspian species. J Great Lakes Res 35:224–231CrossRefGoogle Scholar
  9. Chesson J (1978) Measuring preference in selective predation. Ecology 59:211–215CrossRefGoogle Scholar
  10. Chesson J (1983) The estimation and analysis of preference and its relationship to foraging models. Ecology 64:1297–1304CrossRefGoogle Scholar
  11. Coulas RA, MacIsaac HJ, Dunlop W (1998) Selective predation on an introduced zooplankter (Bythotrephes cederstroemi) by lake herring (Coregonus artedii) in Harp Lake, Ontario. Freshwat Biol 40:343–355CrossRefGoogle Scholar
  12. Fernandez RJ, Rennie MD, Sprules WG (2009) Changes in nearshore zooplankton associated with species invasions and potential effects on larval lake whitefish (Coregonus clupeaformis). Int Rev Hydrobiol 94:226–243CrossRefGoogle Scholar
  13. Findlay DL, Vanni MJ, Paterson M, Mills KH, Kasian SEM, Findlay WJ, Salki AG (2005) Dynamics of a boreal lake ecosystem during a long-term manipulation of top predators. Ecosystems 8:603–618CrossRefGoogle Scholar
  14. Foster SE, Sprules WG (2009) Effects of the Bythotrephes invasion on native predatory invertebrates. Limnol Oceanogr 54:757–769CrossRefGoogle Scholar
  15. Girard RE, Clark BJ, Yan ND, Reid RA, David SM, Ingram RG and Findeis JG (2007) History of chemical, physical and biological methods, sample locations and lake morphometry for the Dorset Environmental Science Centre (1973–2006). Ontario ministry of the environment technical reportGoogle Scholar
  16. Gorokhova E, Hansson S, Hoglander H, Andersen CM (2005) Stable isotopes show food web changes after invasion by the predatory cladoceran Cercopagis pengoi in a Baltic Sea bay. Oecologia 143:251–259PubMedCrossRefGoogle Scholar
  17. Health Canada (2007) Human health risk assessment of mercury in fish and health benefits of fish consumption. Available from Accessed June 2010
  18. Hogan LS, Marschall E, Folt C, Stein RA (2007) How non-native species in Lake Erie influence trophic transfer of mercury and lead to top predators. J Great Lakes Res 33:46–61CrossRefGoogle Scholar
  19. James LAH (2010) The effect of the invasive macroinvertebrate, Bythotrephes longimanus, on cisco (Coregonus artedii) in Ontario shield lakes, Queen’s University, KingstonGoogle Scholar
  20. Jeziorski A, Yan ND, Paterson AM, DeSellas AM, Turner MA, Jeffries DS, Keller B, Weeber RC, McNicol DK, Palmer ME, McIver K, Arseneau K, Ginn BK, Cumming BF, Smol JP (2008) The widespread threat of calcium decline in fresh waters. Science 322:1374–1377PubMedCrossRefGoogle Scholar
  21. Johnson TB, Brown WP, Corry TD, Hoff MH, Scharold JV, Trebitz AS (2004) Lake herring (Coregonus artedi) and rainbow smelt (Osmerus mordax) diets in western Lake Superior. J Great Lakes Res 30:407–413CrossRefGoogle Scholar
  22. Johnston TA, Leggett WC, Bodaly RA, Swanson HK (2003) Temporal changes in mercury bioaccumulation by predatory fishes of boreal lakes following the invasion of an exotic forage fish. Environ Toxicol Chem 22:2057–2062PubMedCrossRefGoogle Scholar
  23. Lasenby DC, Northcote TG, Furst M (1986) Theory, practice, and effects of Mysis relicta introductions to north-american and Scandinavian lakes. Can J Fish Aquat Sci 43:1277–1284CrossRefGoogle Scholar
  24. Legendre P, Legendre L (1998) Numerical ecology. Elsevier Science B. V, AmsterdamGoogle Scholar
  25. MacIsaac HJ, Borbely JVM, Muirhead JR, Graniero PA (2004) Backcasting and forecasting biological invasions of inland lakes. Ecol Appl 14:773–783CrossRefGoogle Scholar
  26. Martin NV, Chapman LJ (1965) Distribution of certain crustaceans and fishes in region of Algonquin Park, Ontario. J Fish Res Board Can 22:969–976CrossRefGoogle Scholar
  27. Mills EL, Ogorman R, Degisi J, Heberger RF, House RA (1992) Food of the alewife (Alosa pseudoharengus) in Lake Ontario before and after the establishment of Bythotrephes cederstroemi. Can J Fish Aquat Sci 49:2009–2019CrossRefGoogle Scholar
  28. Nero RW, Sprules WG (1986) Zooplankton species abundance and biomass in relation to occurrence of Mysis relicta (malacostraca, mysidacea). Can J Fish Aquat Sci 43:420–434CrossRefGoogle Scholar
  29. Orlóci L (1967) An agglomerative method for classification of plant communities. J Ecol 55:193CrossRefGoogle Scholar
  30. Pangle KL, Peacor SD (2006) Non-lethal effect of the invasive predator Bythotrephes longimanus on Daphnia mendotae. Freshwat Biol 51:1070–1078CrossRefGoogle Scholar
  31. Pangle KL, Peacor SD, Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88:402–412PubMedCrossRefGoogle Scholar
  32. Parker Stetter SL, Witzel LD, Rudstam LG, Einhouse DW, Mills EL (2005) Energetic consequences of diet shifts in Lake Erie rainbow smelt (Osmerus mordax). Can J Fish Aquat Sci 62:145–152CrossRefGoogle Scholar
  33. Paterson MJ, Podemski CL, Findlay WJ, Findlay DL, Salki AG (2010) The response of zooplankton in a whole-lake experiment on the effects of a cage aquaculture operation for rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 67:1852–1861CrossRefGoogle Scholar
  34. Post DM, Takimoto G (2007) Proximate structural mechanisms for variation in food-chain length. Oikos 116:775–782CrossRefGoogle Scholar
  35. Prest VK, Douglas RJW (1969) Quaternary geology of Canada. Geology and economic minerals of Canada. Queen’s Printer, Geological Survey of Canada, Ottawa, pp 676–764Google Scholar
  36. Rasmussen JB, Rowan DJ, Lean DRS, Carey JH (1990) Food-chain structure in Ontario lakes determines PCB levels in lake trout (Salvelinus namaycush) and other pelagic fish. Can J Fish Aquat Sci 47:2030–2038CrossRefGoogle Scholar
  37. Rautio M, Tartarotti B (2010) UV radiation and freshwater zooplankton: damage, protection and recovery. Freshwater Rev 3:105–131Google Scholar
  38. R Development Core Team (2008) R: a language and environment for statistical computing. Retrieved from on May 21 2010
  39. Rennie MD, Sprules WG, Vaillancourt A (2010) Changes in fish condition and mercury vary by region, not Bythotrephes invasion: a result of climate change? Ecography 33:471–482Google Scholar
  40. Rusak JA, Yan ND, Somers KM, Cottingham KL, Micheli F, Carpenter SR, Frost TM, Paterson MJ, McQueen DJ (2002) Temporal, spatial and taxonomic patterns of crustacean zooplankton variability in unmanipulated north-temperate lakes. Limnol Oceanogr 47:613–625CrossRefGoogle Scholar
  41. Schulz KL, Yurista PM (1998) Implications of an invertebrate predator’s (Bythotrephes cederstroemi) atypical effects on a pelagic zooplankton community. Hydrobiologia 380:179–193CrossRefGoogle Scholar
  42. Sprules WG (1984) Towards an optimal classification of zooplankton for lake ecosystem studies. Verh Internat Verein Limnol 22:320–325Google Scholar
  43. Strecker AL, Arnott SE (2008) Invasive predator, Bythotrephes, has varied effects on ecosystem function in freshwater lakes. Ecosystems 11:490–503CrossRefGoogle Scholar
  44. Strecker AL, Arnott SE, Yan ND, Girard R (2006) Variation in the response of crustacean zooplankton species richness and composition to the invasive predator Bythotrephes longimanus. Can J Fish Aquat Sci 63:2126–2136CrossRefGoogle Scholar
  45. Swanson HK, Johnston TA, Leggett WC, Bodaly RA, Doucett RR, Cunjak RA (2003) Trophic positions and mercury bioaccumulation in rainbow smelt (Osmerus mordax) and native forage fishes in northwestern Ontario lakes. Ecosystems 6:289–299CrossRefGoogle Scholar
  46. Trippel EA, Beamish FWH (1993) Multiple trophic level structuring in salvelinus coregonus assemblages in boreal forest lakes. Can J Fish Aquat Sci 50:1442–1455CrossRefGoogle Scholar
  47. Vander Zanden MJ, Rasmussen JB (1996) A trophic position model of pelagic food webs: Impact on contaminant bioaccumulation in lake trout. Ecol Monogr 66:451–477CrossRefGoogle Scholar
  48. Vanderploeg HA, Scavia D (1979) Two electivity indices for feeding with special reference to zooplankton grazing. J Fish Res Board Can 36:362–365CrossRefGoogle Scholar
  49. Williamson CE, Olson OG, Lott SE, Walker ND, Engstrom DR, Hargreaves BR (2001) Ultraviolet radiation and zooplankton community structure following deglaciation in Glacier Bay, Alaska. Ecology 82:1748–1760CrossRefGoogle Scholar
  50. Yan ND, Pawson TW (1997) Changes in the crustacean zooplankton community of Harp Lake, Canada, following invasion by Bythotrephes cederstroemi. Freshwat Biol 37:409–425CrossRefGoogle Scholar
  51. Yan ND, Pawson TW (1998) Seasonal variation in the size and abundance of the invading Bythotrephes in Harp Lake, Ontario, Canada. Hydrobiologia 361:157–168CrossRefGoogle Scholar
  52. Yan ND, Keller W, Somers KM, Pawson TW, Girard RE (1996) Recovery of crustacean zooplankton communities from acid and metal contamination: comparing manipulated and reference lakes. Can J Fish Aquat Sci 53:1301–1327CrossRefGoogle Scholar
  53. Yan ND, Girard R, Boudreau S (2002) An introduced invertebrate predator (Bythotrephes) reduces zooplankton species richness. Ecol Lett 5:481–485CrossRefGoogle Scholar
  54. Yan ND, Somers KM, Girard RE, Paterson AM, Keller W, Ramcharan CW, Rusak JA, Ingram R, Morgan GE, Gunn JM (2008) Long-term trends in zooplankton of Dorset, Ontario, lakes: the probable interactive effects of changes in pH, total phosphorus, dissolved organic carbon, and predators. Can J Fish Aquat Sci 65:862–877CrossRefGoogle Scholar
  55. Young JD, Yan ND (2008) Modification of the diel vertical migration of Bythotrephes longimanus by the cold-water planktivore, Coregonus artedi. Freshwat Biol 53:981–995CrossRefGoogle Scholar
  56. Zar JH (1999) Biostatistical analysis. Prentice Hall Inc., TorontoGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Michael D. Rennie
    • 1
    • 4
    Email author
  • Angela L. Strecker
    • 2
  • Michelle E. Palmer
    • 3
  1. 1.Environmental and Life Sciences ProgramTrent UniversityPeterboroughCanada
  2. 2.School of Aquatic and Fishery SciencesUniversity of WashingtonSeattleUSA
  3. 3.Department of BiologyYork UniversityTorontoCanada
  4. 4.Fisheries and Oceans Canada, Freshwater InstituteWinnipegCanada

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