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Increased abundance of the non-indigenous zooplanktivore, Bythotrephes longimanus, is strongly correlated with greater spring prey availability in Canadian Shield lakes

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Abstract

The non-indigenous zooplanktivore, Bythotrephes longimanus, is a large Palaearctic cladoceran that is spreading rapidly in the Great Lakes watershed in North America. As a voracious predator, Bythotrephes can reduce herbivorous cladoceran abundance and diversity; however, the variables that affect its abundance are not well understood. To determine what bottom-up factors are associated with the abundance and seasonal dynamics of established Bythotrephes populations, two Bythotrephes datasets from lakes in south-central Ontario, Canada, were analysed using multiple regression and multivariate analyses: a multi-lake dataset of nine lakes sampled in 2003 and a multi-year dataset of one of these lakes, Harp Lake, sampled from 1994–1998 and 2001–2004. Bottom-up variables tested were Secchi disk depth, epilimnetic temperature, cladoceran (prey) density, total phosphorus, dissolved organic carbon and Chlorophyll a, as well as maximum depth for the multi-lake dataset. In both analyses and datasets, springtime abundance of herbivorous cladocerans was consistently found to be a significant factor associated with Bythotrephes (June–September) abundance; Bythotrephes annual abundance was significantly and positively associated with mean May and June prey abundance, along with mean Secchi disk depth for the multi-lake dataset, and groups of lakes or years with similar Bythotrephes seasonal abundance patterns were predicted by June prey abundance. Additionally, prey availability was the dominant contributor towards changes in weekly Bythotrephes birth rates calculated for two of the study lakes. Our study suggests that prey availability influences Bythotrephes abundance, which provides evidence that Bythotrephes establishment success is affected by the abundance of its prey.

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References

  • 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 Report, 44 pp + appendices

  • Andrew TE, Herzig A (1984) The respiration rate of the resting eggs of Leptodora kindtii (Focke 1844) and Bythotrephes longimanus 1860 (Crustacea, Cladocera) at environmentally encountered temperatures. Oecologia 64:241–244

    Article  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

    Article  Google Scholar 

  • Boudreau SA, Yan ND (2003) The differing crustacean zooplankton communities of Canadian Shield lakes with and without the non-indigenous zooplanktivore Bythotrephes longimanus. Can J Fish Aquat Sci 60:1307–1313

    Article  Google Scholar 

  • 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 Inv 8:1367–1379

    Article  Google Scholar 

  • Brown MA (2006) The ecology of the exotic zooplankter, Bythotrephes longimanus, in a reservoir system: evaluating the role of multiple environmental factors in life-cycle completion. Dissertation, University of Minnesota

  • Burkhardt S, Lehman JT (1994) Prey consumption and predatory effects of an invertebrate predator (Bythotrephes: Cladocera, Cercopagidae) based on phosphorus budgets. Limnol Oceanogr 39:1007–1019

    Article  Google Scholar 

  • Cairns A, Yan ND, Weisz E, Petruniak J, Hoare J (2007) The large, inland lake, Bythotrephes survey—limnology, database design, and presence of Bythotrephes and other pelagic macroinvertebrates in 311 south-central Ontario lakes. Operationalizing CAISN project 1.V, Technical Report #2

  • Coulas RA, MacIsaac HJ, Dunlop W (1998) Selective predation on an introduced zooplankter (Bythotrephes cederstroemi) by lake herring (Coregonus artedii) in Harp Lake, Ontario. Freshw Biol 40:343–355

    Article  Google Scholar 

  • De Mott WR (1980) An analysis of the precision of birth and death rate estimates for egg-bearing zooplankters. In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. Hanover, New Hampshire, USA, pp 337–345

    Google Scholar 

  • 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 46:241–251

    Article  Google Scholar 

  • Foster SE, Sprules WG (2010) Effects of Bythotrephes on the trophic position of native macroinvertebrates. Can J Fish Aquat Sci 67:58–69

    Article  CAS  Google Scholar 

  • Girard R, Reid RA (1990) Dorset Research Centre study lakes: sampling methodology (1986–1989) and lake morphometry. OMOE, Dorset, Canada

    Google Scholar 

  • Gliwicz ZM, Pijanowska J (1989) The role of predation in zooplankton succession. In: Sommer U (ed) Plankton ecology: succession in plankton communities. Springer, Heidelberg, Germany, pp 253–295

    Google Scholar 

  • Goulden CE, Hornig LL (1980) Population oscillations and energy reserves in planktonic cladocera and their consequences to competition. Proc Natl Acad Sci USA 77:1716–1720

    Article  PubMed  CAS  Google Scholar 

  • Grigorovich IA, Pashkova OV, Gromova YF, van Overdijk CDA (1998) Bythotrephes longimanus in the Commonwealth of Independent States: variability, distribution and ecology. Hydrobiologia 379:183–198

    Article  Google Scholar 

  • Hall DJ (1964) An experimental approach to the dynamics of a natural population of Daphnia galeata mendotae. Ecology 45:94–112

    Article  Google Scholar 

  • Hall RI, Yan ND (1997) Comparing annual population growth estimates of the exotic invader Bythotrephes by using sediment and plankton records. Limnol Oceanogr 42:112–120

    Article  Google Scholar 

  • Ingram RG, Girard RE, Clark BJ, Paterson AM, Reid RA, Findeis JG (2006) Dorset Environmental Science Centre: lake sampling methods. Queen’s Printer for Ontario, Toronto, ON, Canada. ISBN 1-4249-2049-3

  • Jarnagin ST, Kerfoot WC, Swan BK (2004) Zooplankton life cycles: direct documentation of pelagic births and deaths relative to diapausing egg production. Limnol Oceanogr 49:1317–1332

    Article  Google Scholar 

  • Johannsson OE, Mills EL, O’ Gorman R (1991) Changes in the nearshore and offshore zooplankton communities in Lake Ontario: 1981–88. Can J Fish Aquat Sci 48:1546–1557

    Article  Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  PubMed  Google Scholar 

  • Lampert W, Fleckner W, Rai H, Taylor BE (1989) Phytoplankton control by grazing zooplankton: a study on the spring clear-water phase. Limnol Oceanogr 31:478–490

    Article  Google Scholar 

  • Langeland A (1978) Effect of fish (Salvelinus alpinus, arctic char) predation on the zooplankton in ten Norwegian lakes. Verh Int Verein Limnol 20:2065–2069

    Google Scholar 

  • Luecke C, Vanni MJ, Magnuson JJ, Kitchell JF, Jacobson PT (1990) Seasonal regulation of Daphnia populations by planktivorous fish—implications for the spring clear-water phase. Limnol Oceanogr 35:1718–1733

    Article  Google Scholar 

  • 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 149:1–21

    Google Scholar 

  • Manca MM, Portogallo M, Brown ME (2007) Shifts in phenology of Bythotrephes longimanus and its modern success in Lago Maggiore as a result of changes in climate and trophy. J Plankton Res 29:515–525

    Article  Google Scholar 

  • Muirhead J, Sprules WG (2003) Reaction distance of Bythotrephes longimanus, encounter rate and index of prey risk for Harp Lake, Ontario. Freshw Biol 48:135–146

    Article  Google Scholar 

  • Muirhead JR, MacIsaac HJ (2011) Evaluation of stochastic gravity model selection for use in estimating non-indigenous species dispersal and establishment. doi:10.1007/s10530-011-0070-3

  • Nilsson NA (1979) Food and habitat of the fish community of the offshore region of Lake Vanern, Sweden. Inst Freshwater Res Dottingholm Rep 58:126–139

    Google Scholar 

  • Nordin LJ, Arts MT, Johannsson OE, Taylor WD (2008) An evaluation of the diet of Mysis relicta using gut contents and fatty acid profiles in lakes with and without the invader Bythotrephes longimanus (Onychopoda, Cercopagidae). Aquat Ecol 42:421–436

    Article  CAS  Google Scholar 

  • Ontario Ministry of the Environment (2003) Approved routine methods reports. E3042, 3422, 3249, 3036, 3147, 3424, 3024, 3386, OMOE, Laboratory Services Branch. Quality Management Unit, Etobicoke, ON

    Google Scholar 

  • Pangle KL, Peacor SD (2009) Light-dependent predation by the invertebrate planktivore Bythotrephes longimanus. Can J Fish Aquat Sci 66:1748–1757

    Article  Google Scholar 

  • Pangle KL, Peacor SD, Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88:402–412

    Article  PubMed  Google Scholar 

  • Polishchuck LV (1995) Direct positive effect of invertebrate predators on birth rate in Daphnia studied with a new method of birth rate analysis. Limnol Oceanogr 40:483–489

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Rivier I (1998) The predatory Cladocera (Onychopoda: Podonidae, Polyphemidae. Backhuys Publishers, Leiden

    Google Scholar 

  • Stenson JAE (1978) Relations between vertebrate and invertebrate zooplankton predators in some arctic lakes. Astarte 11:21–26

    Google Scholar 

  • Straile D, Hälbich A (2000) Life history and multiple antipredator defenses of an invertebrate pelagic predator, Bythotrephes longimanus. Ecology 81:150–163

    Google Scholar 

  • Strecker AL, Arnott SE (2008) Invasive predator, Bythotrephes, has varied effects on ecosystem function in freshwater lakes. Ecosystems 11:490–503

    Article  Google Scholar 

  • 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 63:2126–2136

    Article  Google Scholar 

  • ter Braak CJF, Šmilauer P (2002) CANOCO version 4.5. Biometris—Plant Research International, Wageningen

    Google Scholar 

  • Therriault TW, Grigorovich IA, Cristescu ME, Ketelaars HAM, Viljanen M, Heath DD, MacIsaac HJ (2002) Taxonomic resolution of the genus Bythotrephes Leydig using molecular markers and re-evaluation of its global distribution. Divers Distrib 8:67–84

    Article  Google Scholar 

  • Vanderploeg HA, Liebig JR, Omair M (1993) Bythotrephes predation on Great Lakes’ zooplankton measured by an in situ method: implications for zooplankton community structure. Arch Hydrobiol 12:1–8

    Google Scholar 

  • Wahlström E, Westman E (1999) Planktivory by the predacious cladoceran Bythotrephes longimanus: effects on zooplankton size structure and abundance. Can J Fish Aquat Sci 56:1865–1872

    Google Scholar 

  • Weisz EA, Yan ND (2010) Relative value of limnological, geographic, and human use variables as predictors of the presence of Bythotrephes longimanus in Canadian Shield lakes. Can J Fish Aquat Sci 67:462–472

    Article  CAS  Google Scholar 

  • Wittmann MJ, Lewis MA, Young JD, Yan ND (2011) Temperature-dependent Allee effects in a stage-structured model for Bythotrephes establishment. doi:10.1007/s10530-011-0074-z

  • Yan ND, Pawson TW (1997) Changes in the crustacean zooplankton community of Harp Lake, Canada, following invasion by Bythotrephes cederstroemi. Freshw Biol 37:409–425

    Article  Google Scholar 

  • Yan ND, Pawson TW (1998) Variation in size and abundance of the exotic invader Bythotrephes cederstroemi in Harp Lake, Canada. Hydrobiologia 361:157–168

    Article  Google Scholar 

  • Yan ND, Blukacz A, Sprules WG, Kindy PK, Hackett D, Girard R, Clark BJ (2001) Changes in the zooplankton and the phenology of the spiny water flea, Bythotrephes, following its invasion of Harp Lake, Ontario, Canada. Can J Fish Aquat Sci 58:2341–2350

    Article  Google Scholar 

  • Yan ND, Girard R, Boudreau S (2002) An introduced invertebrate predator (Bythotrephes) reduces zooplankton species richness. Ecol Lett 5:481–485

    Article  Google Scholar 

  • Young JD (2008) Ecological regulators of the life history, morphology, behaviour and abundance of the invasive zooplanktivore Bythotrephes longimanus in south-central Ontario lakes. Dissertation, York University

  • Young JD, Yan ND (2008) Modification of the diel vertical migration of Bythotrephes longimanus by the cold-water planktivore, Coregonus artedi. Freshw Biol 53:981–995

    Article  Google Scholar 

  • Young JD, Loew ER, Yan ND (2009) Examination of direct daytime predation by Coregonus artedi on Bythotrephes longimanus in Harp Lake, Ontario, Canada: No evidence for the refuge hypothesis. Can J Fish Aquat Sci 66:449–459

    Article  Google Scholar 

  • Yurista PM (1992) Embryonic and postembryonic development in Bythotrephes cederstroemi. Can J Fish Aquat Sci 49:1118–1125

    Article  Google Scholar 

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Acknowledgments

We thank Emily Parrott for counting Bythotrephes in the 2003 lake dataset and Brady Yu for counting a portion of the Harp Lake 2003 and Peninsula Lake 2004 datasets. From the OMOE’s Dorset Environmental Science Centre, we thank Andrew Paterson, Robert Girard and Ron Ingram for access to field equipment and Harp Lake Bythotrephes, temperature, chemical and zooplankton data, and Keith Somers for statistical consulting. B. Yu, E. Parrott, Jonathon Hovius, Greg Puncher and Alison Croft provided assistance in the field. We are very grateful for the detailed and helpful comments provided by two reviewers and the editor. Funding for this project was provided by an Ontario Graduate Scholarship in Science and Technology to JDY, and Natural Sciences and Engineering Research Council of Canada grants to ALS and NDY. We also thank Shelley Arnott for guidance and funding.

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Correspondence to Joelle D. Young.

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Young, J.D., Strecker, A.L. & Yan, N.D. Increased abundance of the non-indigenous zooplanktivore, Bythotrephes longimanus, is strongly correlated with greater spring prey availability in Canadian Shield lakes. Biol Invasions 13, 2605–2619 (2011). https://doi.org/10.1007/s10530-011-0077-9

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