Abstract
Invasive species are a major threat to ecosystem structure and function. For example, Bythotrephes cederströmii (Bythotrephes hereafter) invasions have significantly reduced native zooplankton density and biomass, resulting in competitive interactions with zooplanktivorous fishes. Young of year (YOY) walleye (Sander vitreus) are initially zooplanktivorous and have recently been shown to display reduced growth in Bythotrephes-invaded lakes. Here, we combined a bioenergetics model for larval walleye with changes in the zooplankton community following Bythotrephes invasion and predicted reduced larval walleye growth in the presence of Bythotrephes, supporting field observations. The model predicted greater negative impacts on larval walleye growth in oligotrophic compared with mesotrophic lakes, though reduced growth was only significant under oligotrophic conditions. Under Bythotrephes invasion, net energy available to growth over the simulated period was often observed to be negative (indicating mass loss). These combined results from the model suggest that Bythotrephes invasion could potentially lead to walleye recruitment failure, especially in low nutrient environments. This result was insensitive to differences in annual mean water temperatures ranging from 18.5 to 23.5 °C. As YOY growth, survival, and recruitment are ultimately linked to adult abundance and sustainability of managed stocks, our results highlight the potential impacts of Bythotrephes on the sustainability of walleye populations in boreal lakes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Lake total phosphorus data are publicly available from The Ontario Biodiversity Council (https://sobr.ca/indicator/water-quality-inland-lakes/) and walleye presence data are available from the Land Information Ontario repository (https://geohub.lio.gov.on.ca/datasets/lio::aquatic-resource-area-survey-point/about). Zooplankton biomass estimates and bioenergetic model output data are available from the Knowledge Network for Biocomplexity (https://knb.ecoinformatics.org/view/urn%3Auuid%3Aea68a408-8a33-4f2d-a0a3-8b0d848d11b6). All other data and parameters used in models are available in the source literature referenced in the body text of the manuscript.
References
Anderson JT (1988) A review of size dependant survival during pre-recruit stages of fishes in relation to recruitment. J Northwest Atl Fish Sci 8:55–66. https://doi.org/10.2960/j.v8.a6
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. https://doi.org/10.1139/F04-149
Barnett A, Beisner BE (2007) Zooplankton biodiversity and lake trophic state: explanations invoking resource abundance and distribution. Ecology 88:1675–1686. https://doi.org/10.1890/06-1056.1
Barnhisel DR (1991a) The caudal appendage of the cladoceran Bythotrephes cederstroemi as defense against young fish. J Plankton Res 13:529–537. https://doi.org/10.1093/plankt/13.3.529
Barnhisel DR (1991b) Zooplankton spine induces aversion in small fish predators. Oecologia 88:444–450. https://doi.org/10.1007/BF00317591
Bergenius MA, Meekan MG, Robertson DR, McCormick M (2002) Larval growth predicts the recruitment success of a coral reef fish. Oecologia 131:521–525. https://doi.org/10.1007/s00442-002-0918-4
Biro PA, Abrahams MV, Post JR, Parkinson EA (2006) Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates. J Anim Ecol 75:1165–1171. https://doi.org/10.1111/j.1365-2656.2006.01137.x
Boudreau S, 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 60:1307–1313. https://doi.org/10.1139/f03-111
Bunnell DB, Davis BM, Warner DM et al (2011) Planktivory in the changing Lake Huron zooplankton community: Bythotrephes consumption exceeds that of Mysis and fish. Freshw Biol 56:1281–1296. https://doi.org/10.1111/j.1365-2427.2010.02568.x
Bunting L, Leavitt PR, Simpson GL et al (2016) Increased variability and sudden ecosystem state change in Lake Winnipeg, Canada, caused by 20th century agriculture. Limnol Oceanogr 61:2090–2107. https://doi.org/10.1002/lno.10355
Carlson RE (1977) A trophic state index for lakes. Limnol Oceanogr 22:361–369. https://doi.org/10.4319/lo.1977.22.2.0361
Compton JA, Kerfoot CW (2004) Colonizing inland lakes: Consequences of YOY fish ingesting the spiny cladoceran (Bythotrephes cederstroemi). J Great Lakes Res 30:315–326. https://doi.org/10.1016/S0380-1330(04)70394-9
Dabrowski K, Czesny S, Kolkovski S et al (2000) Intensive culture of walleye larvae Produced out of season and during regular season spawning. N Am J Aquac 62:219–224. https://doi.org/10.1577/1548-8454(2000)062%3c0219:icowlp%3e2.3.co;2
Deslauriers D, Chipps SR, Breck JE et al (2017) Fish bioenergetics 4.0: an R-based modeling application. Fisheries 42:586–596. https://doi.org/10.1080/03632415.2017.1377558
Dumitru C, Sprules GW, 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. https://doi.org/10.1046/j.1365-2427.2001.00649.x
Dwivedi AK, Mallawaarachchi I, Alvarado LA (2017) Analysis of small sample size studies using nonparametric bootstrap test with pooled resampling method. Stat Med 36:2187–2205. https://doi.org/10.1002/sim.7263
Fisheries and Oceans Canada (2019a) Survey of Recreational Fishing in Canada, 2015
Fisheries and Oceans Canada (2019b) Freshwater Landings. https://www.dfo-mpo.gc.ca/stats/commercial/land-debarq/freshwater-eaudouce/2019b-eng.htm
Foster SE, Sprules GW (2010) Effects of Bythotrephes on the trophic position of native macroinvertebrates. Can J Fish Aquat Sci 67:58–69. https://doi.org/10.1139/F09-164
Galarowicz TL, Adams JA, Wahl DH (2006) The influence of prey availability on ontogenetic diet shifts of a juvenile piscivore. Can J Fish Aquat Sci 63:1722–1733. https://doi.org/10.1139/F06-073
Galarowicz TL, Wahl DH (2003) Differences in growth, consumption, and metabolism among walleyes from different latitudes. Trans Am Fish Soc 132:425–437. https://doi.org/10.1577/1548-8659(2003)132%3c0425:digcam%3e2.0.co;2
Geisler ME, Rennie MD, Gillis DM, Higgins SN (2016) A predictive model for water clarity following dreissenid invasion. Biol Invasions 18:1989–2006. https://doi.org/10.1007/s10530-016-1146-x
Gillis MK, Walsh MR (2017) Rapid evolution mitigates the ecological consequences of an invasive species (Bythotrephes longimanus) in lakes in Wisconsin. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2017.0814
Graham DM, Sprules GW (1992) Size and species selection of zooplankton by larval and juvenile walleye (Stizostedion vitreum vitreum) in Oneida Lake, New York. Can J Zool 70:2059–2067. https://doi.org/10.1139/z92-277
Grote JD, Wuellner MR, Blackwell BG, Lucchesi DO (2018) Evaluation of potential overwinter mortality of age-0 walleye and appropriate age-1 sampling gear. J Fish Wildl Manag 9:65–74. https://doi.org/10.3996/082017-JFWM-062
Hansen GJA, Ahrenstorff TD, Bethke BJ et al (2020) Walleye growth declines following zebra mussel and Bythotrephes invasion. Biol Invasions 22:1481–1495. https://doi.org/10.1007/s10530-020-02198-5
Houde ED (1967) Food of Pelagic Young of the Walleye, Stizostedion vitreum vitreum, in Oneida Lake, New York. Trans Am Fish Soc 96:17–24. https://doi.org/10.1577/1548-8659(1967)96[17:fopyot]2.0.co;2
Hoxmeier JH, Wahl DH, Hooe ML, Pierce CL (2004) Growth and survival of larval walleyes in response to prey availability. Trans Am Fish Soc 133:45–54. https://doi.org/10.1577/t01-082
Hoxmeier JH, Wahl DH, Brooks RC, Heidinger RC (2006) Growth and survival of age-0 walleye (Sander vitreus): interactions among walleye size, prey availability, predation, and abiotic factors. Can J Fish Aquat Sci 63:2173–2182. https://doi.org/10.1139/F06-087
Jansen W, Gill G, Hann B (2017) Rapid geographic expansion of spiny water flea (Bythotrephes longimanus) in Manitoba, Canada, 2009–2015. Aquat Invasions 12:287–297. https://doi.org/10.3391/ai.2017.12.3.03
Johnson MG, Leach JH, Minns CK, Olver CH (1977) Limnological characteristics of Ontario lakes in relation to associations of walleye (Stizostedion vitreum vitreum), northern pike (Esox lucius), lake trout (Salvelinus namaycush), and smallmouth bass (Micropterus dolomieui). J Fish Res Board Canada 34:1592–1601. https://doi.org/10.1139/f77-224
Johnston TA (1999) Factors affecting food consumption and growth of walleye, Stizostedion vitreum, larvae in culture ponds. Hydrobiologia 400:129–140. https://doi.org/10.1023/A:1003755115000
Johnston TA, Mathias JA (1994) Feeding ecology of walleye, Stizostedion vitreum, larvae: effects of body size, zooplankton abundance, and zooplankton community composition. Can J Fish Aquat Sci 51:2077–2089. https://doi.org/10.1139/f94-210
Jokela A, Arnott SE, Beisner BE (2017) Biotic resistance of impact: a native predator (Chaoborus) influences the impact of an invasive predator (Bythotrephes) in temperate lakes. Biol Invasions 19:1495–1515. https://doi.org/10.1007/s10530-017-1374-8
Jonas JL, Wahl DH (1998) Relative importance of direct and indirect effects of starvation for young walleyes. Trans Am Fish Soc 127:192–205. https://doi.org/10.1577/1548-8659(1998)127%3c0192:riodai%3e2.0.co;2
Kerfoot CW, Hobmeier MM, Yousef F et al (2016) A plague of waterfleas (Bythotrephes): impacts on microcrustacean community structure, seasonal biomass, and secondary production in a large inland-lake complex. Biol Invasions 18:1121–1145. https://doi.org/10.1007/s10530-015-1050-9
Kitchell JF, Stewart DJ, Weininger D (1977) Applications of a bioenergetics model to yellow perch (Perca flavescens) and Walleye (Stizostedion vitreum vitreum). J Fish Res Board Canada 34:1922–1935. https://doi.org/10.1139/f77-258
Kraemer BM, Pilla RM, Woolway RI et al (2021) Climate change drives widespread shifts in lake thermal habitat. Nat Clim Chang 11:521–529. https://doi.org/10.1038/s41558-021-01060-3
Lester NP, Dextrase AJ, Kushneriuk RS et al (2004) Light and temperature: key factors affecting walleye abundance and production. Trans Am Fish Soc 133:588–605. https://doi.org/10.1577/t02-111.1
Ma Q, Jiao Y, Zhou C, Ren Y (2021) Sexual and spatio-temporal variation of Lake Erie Walleye growth and maturity: a consequence of multiple impacting factors. Aquac Fish 6:400–413. https://doi.org/10.1016/j.aaf.2020.06.010
Maberly SC, O’Donnell RA, Woolway RI et al (2020) Global lake thermal regions shift under climate change. Nat Commun. https://doi.org/10.1038/s41467-020-15108-z
Madon SP, Culver DA (1993) Bioenergetics model for larval and juvenile walleyes: an in situ approach with experimental ponds. Trans Am Fish Soc 122:797–813. https://doi.org/10.1577/1548-8659(1993)122%3c0797:bmflaj%3e2.3.co;2
Mainka SA, Howard GW (2010) Climate change and invasive species: double jeopardy. Integr Zool 5:102–111
Malison JA, Held JA (1996) Reproductive biology and spawning. In: Summerfelt RC (ed) Walleye culture manual. North Central Regional Aquaculture Center Publications Office, Iowa State University, Ames, pp 11–18
Massie DL, Hansen GJA, Li Y et al (2021) Do lake-specific characteristics mediate the temporal relationship between walleye growth and warming water temperatures? Can J Fish Aquat Sci 78:913–923. https://doi.org/10.1139/cjfas-2020-0169
Mathias JA, Li S (1982) Feeding habits of walleye larvae and juveniles: comparative laboratory and field studies. Trans Am Fish Soc 111:722–735. https://doi.org/10.1577/1548-8659(1982)111%3c722:fhowla%3e2.0.co;2
Matsuzaki SIS, Lathrop RC, Carpenter SR et al (2021) Climate and food web effects on the spring clear-water phase in two north-temperate eutrophic lakes. Limnol Oceanogr 66:30–46. https://doi.org/10.1002/lno.11584
May CJ, Ludsin SA, Glover DC, Marschall EA (2020) The influence of larval growth rate on juvenile recruitment in Lake Erie walleye (Sander vitreus). Can J Fish Aquat Sci 77:548–555. https://doi.org/10.1139/cjfas-2019-0059
McDonnell KN, Roth BM (2014) Evaluating the effect of pelagic zooplankton community composition and density on larval walleye (Sander vitreus) growth with a bioenergetic-based foraging model. Can J Fish Aquat Sci 71:1039–1049. https://doi.org/10.1139/cjfas-2013-0498
Moore A, Prange M, Bristow B, Summerfelt R (1994) Influence of stocking densities on walleye fry viability in experimental and production tanks. Prog Fish-Cult 56:192–201. https://doi.org/10.1577/1548-8640(1994)056%3c0194:IOSDOW%3e2.3.CO;2
Ontario Biodiversity Council (2021) State of Ontario’s Biodiversity. http://ontariobiodiversitycouncil.ca/sobr. Accessed 5 Apr 2022
Ontario Ministry of Natural Resources and Forestry (2020) Aquatic Resource Area Survey Point. https://geohub.lio.gov.on.ca/datasets/lio::aquatic-resource-area-survey-point/about
Pangle KL, Peacor SD, Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88:402–412. https://doi.org/10.1890/06-0768
Post JR, Evans DO (1989) Size-dependent overwinter mortality of young-of-the-year yellow perch (Perca flavescens): laboratory, in situ enclosure, and field experiments. Can J Fish Aquat Sci 46:1958–1968. https://doi.org/10.1139/f89-246
Rantala HM, Branstrator DK, Hirsch JK et al (2022) Simultaneous invasion decouples zebra mussels and water clarity. Commun Biol. https://doi.org/10.1038/s42003-022-04355-z
Rowe DK, Thorpe JE (1990) Suppression of maturation in male Atlantic salmon (Salmo salar L.) parr by reduction in feeding and growth during spring months. Aquaculture 86:291–313. https://doi.org/10.1016/0044-8486(90)90121-3
Shelton AO, Mangel M (2011) Fluctuations of fish populations and the magnifying effects of fishing. Proc Natl Acad Sci U S A 108:7075–7080. https://doi.org/10.1073/pnas.1100334108
Sorensen ML, Branstrator DK (2017) The North American invasive zooplanktivore Bythotrephes longimanus is less hypoxia-tolerant than the native Leptodora kindtii. Can J Fish Aquat Sci 74:824–832. https://doi.org/10.1139/cjfas-2016-0188
Spear MJ, Walsh JR, Ricciardi A, Jake Vander Zanden M (2021) The Invasion ecology of sleeper populations: prevalence, persistence, and abrupt shifts. Bioscience 71:357–369. https://doi.org/10.1093/biosci/biaa168
Stein SR, Roswell CR, Pothoven SA, Höök TO (2017) Diets and growth of age-0 walleye in a recently recovered population. J Great Lakes Res 43:100–107. https://doi.org/10.1016/j.jglr.2017.03.019
Strecker AL, Arnott SE (2008) Invasive predator, Bythotrephes, has varied effects on ecosystem function in freshwater lakes. Ecosystems 11:490–503. https://doi.org/10.1007/s10021-008-9137-0
Trudel M, Tremblay A, Schetagne R, Rasmussen JB (2000) Estimating food consumption rates of fish using a mercury mass balance model. Can J Fish Aquat Sci 57:414–428. https://doi.org/10.1139/f99-262
Uphoff CS, Schoenebeck CW, Koupal KD et al (2019) Age-0 walleye Sander vitreus display length-dependent diet shift to piscivory. J Freshw Ecol 34:27–36. https://doi.org/10.1080/02705060.2018.1529637
Venturelli PA, Lester NP, Marshall TR, Shuter BJ (2010) Consistent patterns of maturity and density-dependent growth among populations of walleye (Sander vitreus): application of the growing degree-day metric. Can J Fish Aquat Sci 67:1057–1067. https://doi.org/10.1139/F10-041
Walsh JR, Munoz SE, Van Der Zanden MJ (2016) Outbreak of an undetected invasive species triggered by a climate anomaly. Ecosphere. https://doi.org/10.1002/ecs2.1628
Walsh JR, Hansen GJA, Read JS, Vander Zanden MJ (2020) Comparing models using air and water temperature to forecast an aquatic invasive species response to climate change. Ecosphere. https://doi.org/10.1002/ecs2.3137
Wang HY, Einhouse DW, Fielder DG et al (2012) Maternal and stock effects on egg-size variation among walleye Sander vitreus stocks from the Great Lakes region. J Great Lakes Res 38:477–489. https://doi.org/10.1016/j.jglr.2012.06.002
Yan ND, Girard R, Boudreau S (2002) An introduced invertebrate predator (Bythotrephes) reduces zooplankton species richness. Ecol Lett 5:481–485. https://doi.org/10.1046/j.1461-0248.2002.00348.x
Zorn TG, Hayes DB, McCullough DE, Watson NM (2020) Crustacean zooplankton available for larval walleyes in a Lake Michigan embayment. J Great Lakes Res. https://doi.org/10.1016/j.jglr.2020.06.017
Acknowledgements
The authors would like to thank Shelley Arnott for providing zooplankton abundance estimates from various lakes in Northern Ontario generated through the Canadian Aquatic Invasive Species Network (CAISN). The authors would also like to thank the Minnesota Department of Natural Resources Large Lakes Monitoring Program for providing zooplankton abundance estimates from various lakes in Northern Minnesota. Comments from two anonymous reviewers helped improve both the readability and scope of the manuscript. This work was supported by grants from the Quetico Foundation, the Rainy Lakes Fishery Trust, NSERC Discovery, the Canada Research Chair program and Lakehead University.
Author information
Authors and Affiliations
Contributions
Both authors contributed to the design and conception of the study. DG preformed data preparation, analysis, and prepared the first draft of the manuscript. MR provided support to automate results generation, provided comments and edits on subsequent versions of the manuscript and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gartshore, D.J., Rennie, M.D. Decline of young-of-year walleye (Sander vitreus) growth due to Bythotrephes impacts predicted from bioenergetic principles. Biol Invasions 25, 2643–2658 (2023). https://doi.org/10.1007/s10530-023-03065-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-023-03065-9