, Volume 817, Issue 1, pp 379–391 | Cite as

Effect of non-native versus native invaders on macrophyte richness: are carp and bullheads ecological proxies?

  • Przemyslaw G. Bajer
  • Marcus W. Beck
  • Peter J. Hundt


While it is accepted that invasive species are non-native organisms that become abundant and cause ecological damage in areas where they are introduced, the problem of ‘native invaders,’ native species that become excessively abundant due to anthropogenic impacts, is frequently encountered by ecologists. Often, native and non-native invaders occur in sympatry. Understanding relative severity of their impacts and niches they occupy is needed to inform management actions. Here, we quantify relative impact of native (black bullhead) and non-native (common carp) benthic fish on macrophytes species richness in over 200 lakes in North America. The impact of each species was addressed while accounting for the effects of water clarity, depth, lake area, watershed size, shoreline irregularity, land use by humans, abundance of planktivorous fishes, and ecoregion. Using model selection, we show that both species had negative impact on macrophytes richness, but the impact of carp was approximately two times as strong when adjusted for catch rates. We also conducted a principal component analysis followed by permutation procedures, which showed that carp and bullheads often occurred together in shallow, turbid lakes in watershed dominated by human use. Our findings have implications for lake-restoration efforts via carp or bullhead management.


Ameiurus melas Biodiversity Cyprinus carpio Invasive species Lake restoration Eutrophication 



Aaron Rendahl (the University of Minnesota) helped with statistical analyses. Carol Reschke and Donna Perleberg (both at the Minnesota Department of Natural Resources) helped with interpreting aquatic plant data. P. G. Bajer’s salary was supported by a grant from the Environment and Natural Resource Trust Fund to the Minnesota Aquatic Invasive Species Research Center at the University of Minnesota. We thank two anonymous reviewers for providing comments that improved this manuscript.

Supplementary material

10750_2018_3592_MOESM1_ESM.xls (142 kb)
Supplementary material 1 (XLS 142 kb)
10750_2018_3592_MOESM2_ESM.docx (1.5 mb)
Supplementary material 2 (DOCX 1512 kb)


  1. Badiou, P. H. J. & L. G. Goldsborough, 2010. Ecological impacts of an exotic benthivorous fish in large experimental wetlands, Delta Marsh, Canada. Wetlands 30(4): 657–667.CrossRefGoogle Scholar
  2. Bajer, P. G. & P. W. Sorensen, 2010. Recruitment and abundance of an invasive fish, the common carp, is driven by its propensity to invade and reproduce in basins that experience winter-time hypoxia in interconnected lakes. Biological Invasions 12: 1101–1112.CrossRefGoogle Scholar
  3. Bajer, P. G. & P. W. Sorensen, 2015. Effects of common carp on phosphorus concentrations, water clarity, and vegetation density: a whole system experiment in a thermally stratified lake. Hydrobiologia 746: 303–311.CrossRefGoogle Scholar
  4. Bajer, P. G., G. Sullivan & P. W. Sorensen, 2009. Effects of a rapidly increasing population of common carp on vegetative cover and waterfowl in a recently restored Midwestern shallow lake. Hydrobiologia 632: 235–245.CrossRefGoogle Scholar
  5. Bajer, P. G., T. K. Cross, J. D. Lechelt, C. J. Chizinski, M. J. Weber & P. W. Sorensen, 2015a. Across-ecoregion analysis suggests a hierarchy of ecological filters that regulate recruitment of a globally invasive fish. Diversity and Distributions 21: 500–510.CrossRefGoogle Scholar
  6. Bajer, P. G., J. E. Parker, T. K. Cross, P. A. Venturelli & P. W. Sorensen, 2015b. Partial migration to seasonally-unstable habitat facilitates biological invasions in a predator-dominated system. Oikos 124: 1520–1526.CrossRefGoogle Scholar
  7. Bajer, P. G., M. W. Beck, T. K. Cross, J. D. Koch, W. M. Bartodziej & P. W. Sorensen, 2016. Biological invasion by a benthivorous fish reduced the cover and species richness of aquatic plants in most lakes of a large North American ecoregion. Global Change Biology 22: 3937–3947.CrossRefPubMedGoogle Scholar
  8. Barton, K., 2015. MuMIn: Multi-model inference. R package version 1.15.1. [available on internet at].
  9. Bates, D., M. Maechler, B. Bolker, et al., 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.CrossRefGoogle Scholar
  10. Bollen, K. A. & R. W. Jackman, 1990. In Fox, J. & J. S. Long (eds), Regression Diagnostics: An Expository Treatment of Outliers and Influential Cases. Modern Methods of Data Analysis. Sage, Newbury Park: 257–291.Google Scholar
  11. Bourgues, S. & B. T. H. Hart, 2007. Nitrogen removal capacity of wetlands: sediment versus epiphytic biofilms. Water Science and Technology 55: 175–182.CrossRefPubMedGoogle Scholar
  12. Braig, E. C. & D. L. Johnson, 2003. Impact of black bullhead (Ameiurus melas) on turbidity in a diked wetland. Hydrobiologia 490: 11–21.CrossRefGoogle Scholar
  13. Breukelaar, A. W., E. H. R. R. Lammens, J. G. P. K. Breteler & I. Tatrai, 1994. Effects of benthivorous bream (Abramis brama) and carp (Cyprinus Carpio) on sediment resuspension and concentrations of nutrients and Chlorophyll-A. Freshwater Biology 32: 113–121.CrossRefGoogle Scholar
  14. Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multimodel Inference: A practical Information-Theoretic Approach. Springer, New York.Google Scholar
  15. Cahn, A. R., 1929. The effects of carp on a small lake: the carp as a dominant. Ecology 10: 271–274.CrossRefGoogle Scholar
  16. CEC (Commission For Environmental Cooperation), 1997. Ecological Regions of North America: Toward a Common Perspective. CEC, Montreal.Google Scholar
  17. Crivelli, A. J., 1981. The biology of the common carp, Cyprinus carpio L. in the Camargue, southern France. Journal of fish Biology 18: 271–290.CrossRefGoogle Scholar
  18. Fischer, J. R., R. M. Krogman & M. C. Quist, 2013. Influences of native and non-native benthivorous fishes on aquatic ecosystem degradation. Hydrobiologia 711: 187–199.CrossRefGoogle Scholar
  19. Haas, K., U. Kohler, S. Diehl, P. Kohler, S. Dietrich, S. Holler, A. Jaensch, M. Niedermaier & J. Vilsmeier, 2007. Influence of fish on habitat choice of water birds: a whole system experiment. Ecology 88: 2915–2925.CrossRefPubMedGoogle Scholar
  20. Hanson, M. A. & M. G. Butler, 1994. Responses of plankton, turbidity, and macrophytes to biomanipulation in a shallow prairie lake. Canadian Journal of Fisheries and Aquatic Sciences 51: 1180–1188.CrossRefGoogle Scholar
  21. Hanson, M. A., B. R. Herwig, K. D. Zimmer & N. Hansel-Welch, 2017. Rehabilitation of shallow lakes: time to adjust expectations? Hydrobiologia 787: 45–59.CrossRefGoogle Scholar
  22. Heiskary, S. & B. Wilson, 2008. Minnesota’s approach to lake nutrient criteria development. Lake and Reservoir Management 24: 282–297.CrossRefGoogle Scholar
  23. Huser, B. J., P. G. Bajer, C. J. Chizinski & P. W. Sorensen, 2016. Effects of common carp (Cyprinus carpio) on sediment mixing depth and mobile phosphorus mass in the active sediment layer of a shallow lake. Hydrobiologia 763: 23–33.CrossRefGoogle Scholar
  24. Kulhanek, S. A., B. Leung & A. Ricciardi, 2011a. Using ecological niche models to predict the abundance and impact of invasive species: application to the common carp. Ecological Applications 21: 203–213.CrossRefPubMedGoogle Scholar
  25. Kulhanek, S. A., B. Leung & A. Ricciardi, 2011b. Is invasion history a useful tool for predicting the impacts of the world’s worst aquatic invasive species? Ecological Applications 21: 189–202.CrossRefPubMedGoogle Scholar
  26. Lathrop, R. C., D. S. Liebl & K. Welke, 2013. Carp removal to increase water clarity in shallow eutrophic Lake Wingra. Lakeline 33: 23–30.Google Scholar
  27. Leunda, P. M., J. Oscoz, B. Elvira, A. Agorreta, S. Perea & R. Miranda, 2008. Feeding habits of the exotic black bullhead Ameiurus melas (Rafinesque) in the Iberian Peninsula: first evidence of direct predation on native fish species. Journal of Fish Biology 73: 96–114.CrossRefGoogle Scholar
  28. Lechelt, J. D., M. J. Kocian & P. G. Bajer, 2017. Low downstream dispersal of young-of-year common carp from marshes into lakes in the Upper Mississippi River region and its implications for integrated pest management strategies. Management 8(4): 485–495.Google Scholar
  29. Lougheed, V. L., B. Crosbie & P. Chow-Fraser, 1998. Predictions on the effect of common carp (Cyprinus carpio) exclusion on water quality, zooplankton, and submergent macrophytes in a Great Lakes wetland. Canadian Journal of Fisheries and Aquatic Sciences 55(5): 1189–1197.CrossRefGoogle Scholar
  30. Matsuzaki, S. S., N. Usio, N. Takamura & I. Washitani, 2009. Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis. Oecologia 158(4): 673–686.CrossRefPubMedGoogle Scholar
  31. McCune, B. & J. B. Grace, 2002. Analysis of Ecological Communities. MjM Software Design, Gleneden Beach.Google Scholar
  32. MNDNR (Minnesota Department of Natural Resources), 1993. Manual of Instructions for Lake Survey. MNDNR, Section of Fisheries, Special Publication 147, St. Paul.Google Scholar
  33. Moyle, J. B. & J. Kuehn, 1964. Carp, a sometimes villain. In Linduska, J. P. (ed.), Waterfowl Tomorrow. U. S. Department of Interior, Washington, D. C: 635–642.Google Scholar
  34. Nikolsky, G. V., 1963. The Ecology of Fishes. Academic Press, London.Google Scholar
  35. Omernik, J. M., 2004. Perspectives on the nature and definition of global regions. Environmental Management 34: 27–36.CrossRefGoogle Scholar
  36. Parkos, J. J., V. J. Santucci & D. H. Wahl, 2003. Effects of adult common carp (Cyprinus carpio)on multiple trophic levels in shallow mesocosms. Canadian Journal of Fisheries and Aquatic Sciences 60(2): 182–192.CrossRefGoogle Scholar
  37. Radomski, P., & D. Perleberg, 2012. Application of a versatile aquatic macrophyte integrity index for Minnesota lakes. Ecological indicators 20: 252–268.CrossRefGoogle Scholar
  38. RStudio Team, 2015. RStudio: Integrated Development for R. RStudio, Inc., Boston, MA URL
  39. Repsys, A. J., R. L. Applegate & D. C. Hales, 1976. Food and food selectivity of black bullhead, Ictalurus melas, in Lake Poinsett, South-Dakota. Journal of the Fisheries Research Board of Canada 33: 768–775.CrossRefGoogle Scholar
  40. Schrage, L. J. & J. A. Downing, 2004. Pathways of increased water clarity after fish removal from Ventura Marsh; a shallow, eutrophic wetland. Hydrobiologia 511: 215–231.CrossRefGoogle Scholar
  41. Shackelford, N., M. Renton, M. P. Perring & R. J. Hobbs, 2013. Modeling disturbance-based native invasive species control and its implications for management. Ecological Applications 23: 1331–1344.CrossRefPubMedGoogle Scholar
  42. Sibbing, F. A., J. W. M. Osse & A. Terlouw, 1986. Food handling in the carp (Cyprinus carpio)—its movement patterns, mechanisms and limitations. Journal of Zoology 210: 161–203.CrossRefGoogle Scholar
  43. Vestergaard, O. & K. Send-Jensen, 2000. Aquatic macrophyte richness in Danish lakes in relation to alkalinity, transparency and lake area. Canadian Journal of Fisheries and Aquatic Sciences 57: 2022–2031.CrossRefGoogle Scholar
  44. Vila, M. & J. Weiner, 2004. Are invasive plant species better competitors than native plant species? evidence from pair-wise experiments. Oikos 105: 229–238.CrossRefGoogle Scholar
  45. Vilizzi, L., A. S. Tarkan & G. H. Copp, 2015. Experimental evidence from causal criteria analysis for the effects of common carp Cyprinus carpio on freshwater ecosystems: a global perspective. Revievs in Fisheries Science and Aquaculture 23: 253–290.CrossRefGoogle Scholar
  46. Weber, M. J. & M. L. Brown, 2011. Relationships among invasive common carp, native fishes and physicochemical characteristics in upper Midwest (USA) lakes. Ecology of Freshwater Fish 20: 270–278.CrossRefGoogle Scholar
  47. Wilson, J. N., 1958. The limnology of certain prairie lakes in Minnesota. American Midland Naturalist 59(2): 418–437.CrossRefGoogle Scholar
  48. Zambrano, L., M. Scheffer & M. Martinez-Ramos, 2001. Catastrophic response of lakes to benthivorous fish introduction. Oikos 94: 344–350.CrossRefGoogle Scholar
  49. Zuur, A. F., E. N. Ieno, N. J. Walker, A. A. Saveliev & G. M. Smith, 2009. Mixed Effects Models and Extensions in Ecology with R. Springer, New York.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Przemyslaw G. Bajer
    • 1
  • Marcus W. Beck
    • 2
  • Peter J. Hundt
    • 1
  1. 1.University of MinnesotaSt. PaulUSA
  2. 2.Southern California Coastal Water Research ProjectCosta MesaUSA

Personalised recommendations