Ecosystems

, Volume 11, Issue 3, pp 490–503 | Cite as

Invasive Predator, Bythotrephes, has Varied Effects on Ecosystem Function in Freshwater Lakes

Article

Abstract

Bythotrephes longimanus is an invertebrate predator that has invaded the North American Great Lakes and a number of inland lakes, where it preys on crustacean zooplankton. We examined the effect of Bythotrephes on two measures of ecosystem function during a four-month observational study of freshwater lakes on the boreal shield. Bythotrephes-invaded lakes had significantly lower epilimnetic zooplankton abundance and production compared to reference lakes. On average, Bythotrephes consumed 34% of zooplankton production when it was present in lakes. There was some evidence of changes in the timing of zooplankton production, as well as shifts to cooler, less productive habitats, which may lessen the overall effect of the invader on the transfer of energy to higher trophic levels. We experimentally demonstrated a weak trophic cascade where invader predation reduced zooplankton biomass, and subsequently increased phytoplankton growth. However, the response was small in magnitude and not biologically relevant at the whole lake-scale. The most conspicuous effect of Bythotrephes that we measured was a diversion of energy away from native predators at higher trophic levels.

Keywords

invasive species ecosystem function crustacean zooplankton Bythotrephes freshwater lakes secondary production zooplankton grazing 

Notes

Acknowledgments

This project benefited from discussions with Ora Johannsson, Michael Arts, Beatrix Beisner, Norman Yan, Jon Hovius, Joelle Young, Sophie Foster, Gary Sprules, William Taylor, Lisa Nordin, and Robert Girard. We thank B. Beisner, O. Johannsson, J. Young, Michael Vanni, and two anonymous reviewers for comments on the manuscript. We are grateful to the Ontario Ministry of Natural Resources for providing fish data. We would also like to thank J. Hovius, Emily Parrott, and Greg Puncher for assistance in the field, and E. Parrott for enumerating the Bythotrephes samples. Funding for this project was provided by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to SEA and Post-Graduate Scholarship to ALS, the Department of Fisheries and Oceans Canada, the Ontario Ministry of the Environment, and Queen’s University School of Graduate Studies and Research. Logistical support and water chemistry was provided by the Dorset Environmental Science Centre.

Supplementary material

References

  1. Allan JD. 1976. Life history patterns in zooplankton. Am Nat 110:165–80CrossRefGoogle Scholar
  2. Allen G, Yan ND, Geiling WT 1994. ZEBRA2 – Zooplankton enumeration and biomass routines for APIOS: a semi-automated sample processing system for zooplankton ecologists. Ontario Ministry of Environment and Energy, Dorset, ONGoogle Scholar
  3. Beauchamp DA, Sergeant CJ, Mazur MM, Scheuerell JM, Schindler DE, Scheuerell MD, Fresh KL, Seiler DE, Quinn TP. 2004. Spatial-temporal dynamics of early feeding demand and food supply for sockeye salmon fry in Lake Washington. Trans Am Fish Soc 133: 1014–32CrossRefGoogle Scholar
  4. Borgmann U, Shear H, Moore J. 1984. Zooplankton and potential fish production in Lake Ontario. Can J Fish Aquat Sci 41: 1303–9CrossRefGoogle 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: 1307–13CrossRefGoogle Scholar
  6. Branstrator DK, Brown ME, Shannon LJ, Thabes M, Heimgartner K. 2006. Range expansion of Bythotrephes longimanus in North America: evaluating habitat characteristics in the spread of an exotic zooplankter. Biol Invas 8: 1367–79CrossRefGoogle Scholar
  7. Brooks ML, D’Antonio CM, Richardson DM, Grace JB, Keeley JE, DiTomaso JM, Hobbs RJ, Pellant M, Pyke D. 2004. Effects of alien plants on fire regimes. BioScience 54: 677–88CrossRefGoogle Scholar
  8. Chick JH, van den Avyle MJ. 1999. Zooplankton variability and larval striped bass foraging: evaluating potential match/mismatch regulation. Ecol Appl 9: 320–34CrossRefGoogle Scholar
  9. Culver DA, Boucherle MM, Bean DJ, Fletcher JW. 1985. Biomass of freshwater crustacean zooplankton from length-weight regressions. Can J Fish Aquat Sci 42: 1380–90Google Scholar
  10. Cyr H. 1998. Cladoceran- and copepod-dominated zooplankton communities graze at similar rates in low productivity lakes. Can J Fish Aquat Sci 55: 414–22CrossRefGoogle Scholar
  11. Davis BM, Todd TN. 1998. Competition between larval lake herring (Coregonus artedi) and lake whitefish (Coregonus clupeaformis) for zooplankton. Can J Fish Aquat Sci 55: 1140–8CrossRefGoogle Scholar
  12. Downing JA 1984. Assessment of secondary production: the first step. In: Downing JA, Rigler FH (Eds) A manual on the methods for the assessment of secondary productivity in freshwaters. Blackwell Scientific Publications, Oxford, UK, pp 1–18Google Scholar
  13. Dumitru C, Sprules WG, Yan ND. 2001. Impact of Bythotrephes longimanus on zooplankton assemblages of Harp Lake, Canada: an assessment based on predator consumption and prey production. Freshw Biol 46: 241–51CrossRefGoogle Scholar
  14. Elser JJ, Goldman CR. 1991. Zooplankton effects on phytoplankton in lakes of contrasting trophic status. Limnol Oceanogr 36: 64–90Google Scholar
  15. Elser JJ, Sterner RW, Galford AE, Chrzanowski TH, Findlay DL, Mills KH, Paterson MJ, Stainton MP, Schindler DW. 2000. Pelagic C:N:P stoichiometry in a eutrophied lake: responses to a whole-lake food-web manipulation. Ecosystems 3: 293–307CrossRefGoogle Scholar
  16. Hairston NG Jr, Walton WE. 1986. Rapid evolution of a life history trait. Proc Natl Acad Sci USA 83: 4831–3PubMedCrossRefGoogle Scholar
  17. Hovius JT, Beisner BE, McCann KS. 2006. Epilimnetic rotifer community responses to Bythotrephes longimanus invasion in Canadian Shield lakes. Limnol Oceanogr 51: 1004–12CrossRefGoogle Scholar
  18. Jarnagin ST, Swan BK, Kerfoot WC. 2000. Fish as vectors in the dispersal of Bythotrephes cederstroemi: diapausing eggs survive passage through the gut. Freshw Biol 43: 579–89Google Scholar
  19. Jeppesen E, Jensen JP, Jensen C, Faafeng BA, Hessen DO, Søndergaard M, Lauridsen T, Brettum P, Christoffersen K. 2003. The impact of nutrient state and lake depth on top-down control in the pelagic zone of lakes: a study of 466 lakes from the temperate zone to the Arctic. Ecosystems 6: 313–25CrossRefGoogle Scholar
  20. Jin EH, Sprules WG. 1990. Distribution and abundance of Bythotrephes cederstroemi (Cladocera: Cercopagidae) in the St. Lawrence Great Lakes. Verh Int Verein Theor Angew Limnol 24: 383–5Google Scholar
  21. Kuns MM, Sprules WG. 2000. Zooplankton production in Lake Ontario: a multistrata approach. Can J Fish Aquat Sci 57: 2240–7CrossRefGoogle Scholar
  22. Lampert W. 1989. The adaptive significance of diel vertical migration of zooplankton. Funct Ecol 3: 21–7CrossRefGoogle Scholar
  23. Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA. 2001. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294: 804–8PubMedCrossRefGoogle Scholar
  24. MacIsaac HJ, Ketelaars HAM, Grigorovich IA, Ramcharan CW, Yan ND. 2000. Modeling Bythotrephes longimanus invasions in the Great Lakes basin based on its European distribution. Arch Hydrobiol 149: 1–21Google Scholar
  25. McCauley E 1984. The estimation of the abundance and biomass of zooplankton in samples. In: Downing JA, Rigler FH (Eds) A manual on the methods for the assessment of secondary productivity in freshwaters. Blackwell Scientific Publications, Oxford, UK, pp 228–65Google Scholar
  26. Millenium Ecosystem Assessment. 2005. Ecosystems and human well-being: biodiversity synthesis. Washington, DC: World Resources InstituteGoogle Scholar
  27. Milne SW, Shuter BJ, Sprules WG. 2005. The schooling and foraging ecology of lake herring (Coregonus artedi) in Lake Opeongo, Ontario, Canada. Can J Fish Aquat Sci 62: 1210–8CrossRefGoogle Scholar
  28. Oyadomari JK, Auer NA. 2004. Inshore-offshore distribution of larval fishes in Lake Superior off the western coast of the Keweenaw Peninsula, Michigan. J Great Lakes Res 30(Suppl. 1): 369–84Google Scholar
  29. Paloheimo JE. 1974. Calculations of instantaneous birth rate. Limnol Oceanogr 19: 692–4Google Scholar
  30. Pangle KL, Peacor SD. 2006. Non-lethal effect of the invasive predator Bythotrephes longimanus on Daphnia mendotae. Freshw Biol 51: 1070–8CrossRefGoogle Scholar
  31. Pangle KL, Peacor SD, Johannsson OE. 2007. Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88: 402–12PubMedCrossRefGoogle Scholar
  32. Pérez-Fuentetaja A, McQueen DJ, Yan ND, Dillon PJ. 2000. Zooplankton biomass rarely improves predictions of chlorophyll concentration in Canadian Shield lakes that vary in pH. Aquat Ecol 34: 127–36CrossRefGoogle Scholar
  33. Ramcharan CW, Pérez-Fuentetaja A, McQueen DJ, Yan ND, Demers E, Rusak JA. 2001. Dynamics of zooplankton productivity under two different predatory regimes. Arch Hydrobiol Special Issues: Adv Limnol 56: 151–69Google Scholar
  34. Rudstam LG, Magnuson JJ. 1985. Predicting the vertical distribution of fish populations: analysis of cisco, Coregonus artedii, and yellow perch, Perca flavescens. Can J Fish Aquat Sci 42: 1178–88CrossRefGoogle Scholar
  35. Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH. 2000. Global biodiversity scenarios for the year 2100. Science 287: 1770–4PubMedCrossRefGoogle Scholar
  36. Sarnelle O, Knapp RA. 2005. Nutrient recycling by fish versus zooplankton grazing as drivers of the trophic cascade in alpine lakes. Limnol Oceanogr 50: 2032–42CrossRefGoogle Scholar
  37. Sherwood GD, Kovecses J, Hontela A, Rasmussen JB. 2002. Simplified food webs lead to energetic bottlenecks in polluted lakes. Can J Fish Aquat Sci 59: 1–5CrossRefGoogle Scholar
  38. Simon KS, Townsend CR. 2003. Impacts of freshwater invaders at different levels of ecological organisation, with emphasis on salmonids and ecosystem consequences. Freshw Biol 48: 982–94CrossRefGoogle Scholar
  39. Sommer U, Sommer F, Santer B, Jamieson B, Boersma M, Becker C, Hansen T. 2001. Complementary impact of copepods and cladocerans on phytoplankton. Ecol Lett 4: 545–50CrossRefGoogle Scholar
  40. Sprules WG 1980. Zoogeographic patterns in the size structure of zooplankton communities, with possible applications to lake ecosystem modeling and management. In: Kerfoot WC (Ed) Evolution and ecology 6of zooplankton communities. University Press of New England, Hanover, NH, pp 642–56Google Scholar
  41. StatSoft. 2001. STATISTICA 6. Tulsa, OK, USA: StatSoft IncGoogle Scholar
  42. Strecker AL, Arnott SE. 2005. Impact of Bythotrephes invasion on zooplankton communities in acid-damaged and recovered lakes on the Boreal Shield. Can J Fish Aquat Sci 62: 2450–62CrossRefGoogle Scholar
  43. 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: 2126–36CrossRefGoogle Scholar
  44. Threlkeld ST. 1988. Planktivory and planktivore biomass effects on zooplankton, phytoplankton, and the trophic cascade. Limnol Oceanogr 33: 1362–75CrossRefGoogle Scholar
  45. Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E. 1998. Quantifying threats to imperiled species in the United States. BioScience 48: 607–15CrossRefGoogle Scholar
  46. Yan ND, Blukacz A, Sprules WG, Kindy PK, Hackett D, Girard RE, Clark BJ. 2001. Changes in zooplankton and the phenology of the spiny water flea, Bythotrephes, following its invasion of Harp Lake, Ontario, Canada. Can J Fish Aquat Sci 58: 2341–50CrossRefGoogle Scholar
  47. Yan ND, Girard RE, Boudreau S. 2002. An introduced invertebrate predator (Bythotrephes) reduces zooplankton species richness. Ecol Lett 5: 481–5CrossRefGoogle Scholar
  48. Yan ND, Mackie GL. 1987. Improved estimation of the dry weight of Holopedium gibberum (Crustacea, Cladocera) using clutch size, a body fat index, and lake water total phosphorus concentration. Can J Fish Aquat Sci 44: 382–9CrossRefGoogle Scholar
  49. Yan ND, Pawson TW. 1997. Changes in the crustacean zooplankton community of Harp Lake, Canada, following invasion by Bythotrephes cederstroemi. Freshw Biol 37: 409–25CrossRefGoogle Scholar
  50. Young JD, Yan ND. 2008. Modification of the diel vertical migration of Bythotrephes longimanus by the cold-water planktivore, Coregonus artedi. Freshw Biol doi: 10.1111/j.1365-2427.2008.01954.x
  51. 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: 1017–28CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Department of BiologyQueen’s UniversityKingstonCanada
  2. 2.Department of Ecology & Evolutionary BiologyUniversity of TorontoTorontoCanada

Personalised recommendations