Abstract
The reproductive status of walleye (Sander vitreus) and lake whitefish (Coregonus clupeaformis) is largely unstudied in the northern extent of their ranges. Tathlina Lake and Kakisa Lake are large, shallow lakes in the Northwest Territories, Canada, supporting important commercial and subsistence fisheries for these species while being threatened by climate change. Fish were sampled in both lakes across multiple years in the spring and autumn to assess differences in reproductive status in the pre- and post-spawning periods for both species. Condition factor (K), gonadosomatic index (GSI), liversomatic index (LSI), and fecundity were calculated, and plasma samples were also taken from each fish to determine levels of reproductive hormones, specifically 17β-estradiol in females, and 11-ketotestosterone in males. Significant temporal (intra- and interannual) and spatial (between lakes) variation was found for both species and both sexes for all metrics. Expected differences in hormones and indices of reproductive success between pre- and post- spawning periods were demonstrated. When compared with previously published data, a latitudinal gradient for LSI, GSI and fecundity was evident for walleye, but not for lake whitefish. The differences in the reproductive biology of lake whitefish and walleye in these two neighbouring lakes highlights limitations in the use of a reference lake approach in biomonitoring studies. The data in this study can be used and expanded upon to provide information for the sustainable management of these fish stocks for the future.
Similar content being viewed by others
Availability of data and material
Data available on request from the authors.
References
Alonso-Fernández A, Vallejo AC, Rey FS, Murua H, Trippel EA (2009) Fecundity estimation of Atlantic cod (Gadus morhua) and haddock (Melanogrammus aeglefinus) of Georges Bank: application of the autodiametric method. Fish Res 99:47–54
Anderson JC (2013) The effects of hydroxypropyl-β-Cyclodextrin on the American Flagfish (Jordanella floridae) over one complete life-cycle. Dissertation, University of Ontario Institute of Technology, Oshawa, Ontario, Canada
Barrett TJ, Brasfield SM, Carroll LC, Doyle MA, Van Den Heuvel M, Munkittrick K (2015) Reproductive strategies and seasonal changes in the somatic indices of seven smallbodied fishes in Atlantic Canada in relation to study design for environmental effects monitoring. Environ Monit Assess 187:305–317
Blanck A, Lamouroux N (2007) Large-scale intraspecific variation in life-history traits of European freshwater fish. J Biogeogr 34:862–875
Bowron LK, Munkittrick KR, McMaster ME, Tetreault G, Hewitt LM (2009) Response of white sucker (Catostomus commersoni) to 20 years of process and waste treatment changes at a bleached Kraft pulp mill and to mill shutdown. Aquat Toxicol 95:117–132
Brook RK, Kutz SJ, Veitch AM, Popko RA, Elkin BT, Guthrie G (2009) Fostering community based-wildlife health monitoring and research in the Canadian north. EcoHealth 6:266–278
Casselman SJ, Schulte-Hostedde AI (2004) Reproductive roles predict sexual dimorphism in internal and external morphology of lake whitefish. Coregonus clupeaformis. Ecol Freshw Fish 13:217–222
Chavarie L, Howland K, Venturelli P, Kissinger BC, Tallman R, Tonn W (2016) Life-history variation among four shallow-water morphotypes of lake trout from Great Bear Lake, Canada. J Great Lakes Res 42(2):193–203
Dahle R, Taranger GL, Karlsen O, Kjesbu OS, Norberg B (2003) Gonadal development and associated changes in liver size and sexual steroids during the reproductive cycle of captive male and female Atlantic cod (Gadus morhua L.). Comp Biochem Phys A 136:641–653
De Vlaming VL (1972) Environmental control of teleost reproductive cycles: a brief review. J Fish Biol 4:131–140
De Vlaming VL (1975) Effects of photoperiod and temperature on gonadal activity in the cyprinid teleost, Notemigonus crysoleucas. Biol Bull 148(3):402–415
Depla I, Jung A-V, Baures E, Clement M, Thomas O (2009) Impacts of climate change on surface water quality in relation to drinking water production. Environ Int 35(8):1225–1233
DFO (2010) Assessment of Walleye (Sander vitreus) from Tathlina Lake, Northwest Territories. DFO Canadian Science Advisory Secretariat Science Advisory Report. 2010/035
DFO (2020) Northwest Territories restricted activity timing windows for the protection of fish and fish habitat. URL https://www.dfo-mpo.gc.ca/pnw-ppe/timing-periodes/nwt-eng.html
Environment Canada (2010) Pulp and paper environmental effects monitoring (EEM) technical guidance document, EEM. Environment Canada, Ottawa, Ontario
Feiner ZS, Wang HY, Einhouse DW, Jackson JR, Rutherford ES, Schelb C, Vandergoot CS, Zorn TG, Höök TO (2016) Thermal environment and maternal effects shape egg size in a freshwater fish. Ecosphere 7(5):e01304
Frick WF, Reynolds DS, Kunz TH (2010) Influence of climate and reproductive timing on demography of little brown myotis Myotis lucifugus. J Anim Ecol 79:128–136
Ghaffari H, Ardalan AA, Sahafi HH, Babaei MM, Abdollahi R (2011) Annual changes in gonadosomatic index (GSI), hepatosomatic index (HSI) and condition factor (K) of largescale tonguesole Cynoglossus arel (Bloch and Schneider, 1801) in the coastal waters of Bandar Abbas, Persian Gulf. Aust J Basic Appl Sci 5:1640–1646
Gillio Meina E, Lister A, Bosker T, Servos M, Munkittrick K, MacLatchy D (2013) Effects of 17α- ethinylestradiol (EE2) on reproductive endocrine status in mummichog (Fundulus heteroclitus) under differing salinity and temperature conditions. Aquat Toxicol 134–135:92–103
Grau A, Saborido-Rey F, Pastor E, Palmer M, Massutí-Pascual E, Quetglas A, Riera I, Morales-Nin B (2016) Reproductive strategy of common dentex Dentex dentex: management implications. Mediterr Mar Sci 17(2):552–566
Greenbank J (1945) Limnological conditions in ice-covered lakes, especially as related to winter-kill of fish. Ecol Monogr 15(4):343–392
Harrison G (2017) Reproductive characterization of walleye (Sander vitreus) and lake whitefish (Coregonus clupeaformis) in Tathlina Lake, NT. Dissertation, Wilfrid Laurier University, Waterloo, Ontario
Healey MC, Dietz K (1984) Variation in fecundity of lake whitefish (Coregonus clupeaformis) from lesser slave and Utikuma Lakes in Northern Alberta. Copeia 1984(1):238–242
Henderson BA, Wong JL, Nepszy SJ (1996) Reproduction of walleye in Lake Erie: allocation of energy. Can J Fish Aquat Sci 53:127–133
Johnston TA, Lysack W, Leggett WC (2012a) Abundance, growth, and life history characteristics of sympatric walleye (Sander vitreus) and sauger (Sander canadensis) in Lake Winnipeg, Manitoba. J Great Lakes Res 38:35–46
Johnston TA, Wong DM-M, Moles MD, Wiegand MD, Casselman JM, Leggett WC (2012b) Reproductive allocation in exploited lake whitefish (Coregonus clupeaformis) and walleye (Sander vitreus) populations. Fish Res 125–126:225–234
Kaufman SD, Johnston TA, Leggett WC, Moles MD, Casselman JM, Schulte-Hostedde AI (2007) Relationships between body condition indices and proximate composition in adult walleyes. T Am Fish Soc 136:1566–1576
Kennedy WA (1962) A report on Tathlina and Kakisa lakes – 1946. Manuscript reports of the fisheries research board of Canada (biological) 721. 24 p
Kjesbu OS, Holm JC (1994) Oocyte recruitment in first-time spawning Atlantic cod (Gadus morhua) in relation to feeding regime. Can J Fish Aquat Sci 51:1893–1898
Kjesbu OS, Klungsøyr J, Kryvi H, Witthames PR, Greer Walker M (1991) Fecundity, atresia, and egg size of captive Atlantic cod (Gadus morhua) in relation to proximate body composition. Can J Fish Aquat Sci 48:2333–2343
Lambert Y, Dutil J-D (2000) Energetic consequences of reproduction in Atlantic cod (Gadus morhua) in relation to spawning level of somatic energy reserves. Can J Fish Aquat Sci 57(4):815-825
Landry CA, Steel SL, Manning S, Cheek AO (2007) Long-term hypoxia suppresses reproductive capacity in the estuarine fish, Fundulus grandis. Comp Biochem Phys 148:317–323
Leggett WC, Carscadden JE (1978) Latitudinal variation in reproductive characteristics of American shad (Alosa sapidissima): evidence for population specific life history strategies in fish. J Fish Res Board Can 35:1469–1478
Mackenzie-Grieve JL, Post JR (2006) Projected impacts of climate warming on production of lake trout (Salvelinus namaycush) in southern Yukon lakes. Can J Fish Aquat Sci 63:780–797
Malison JA, Held JA (1996) Reproduction and spawning in walleye (Stizostedion vitreum). J Appl Ichthyol 12:153–156
Malison JA, Procarione LS, Barry TP, Kapuscinski AR, Kayes TB (1994) Endocrine and gonadal changes during the annual reproductive cycle of the freshwater teleost, Stizostedion vitreum. Fish Physio Biochem 13:473–484
Marshall CT, Yaragina NA, Lambert Y, Kjesbu OS (1999) Total lipid energy as a proxy for total egg production by fish stocks. Nature 402:288–290
McMahon TE, Terrell JW, Nelson PC (1984) Habitat suitability information: Walleye. U.S. Fisheries and Wildlife Services. (FWS/OBS-82/10.56). Western Energy and Land Use Team, Division of Biological Services, Research and Development, Fish and Wildlife Service, Washington, DC., pp 1–43
McMaster ME, Munkittrick KR, Van Der Kraak GJ (1992) Protocol for measuring circulating levels of gonadal sex steroids in fish. Can Tech Rep Fish Aquat Sci 1836:29p
McMaster ME, Jardine JJ, Ankley GT, Benson WH, Greeley MS, Gross TS, Guillette LJ, MacLatchy DL, Orlando EF, Van der Kraak GJ, Munkittrick KR (2001) Inter-laboratory study on the use of steroid hormones examining endocrine disruption. Environ Toxicol Chem 20(9):2081–2087
Moles MD, Johnston TA, Robinson BW, Leggett WC, Caselman JM (2008) Is gonadal investment in walleye (Sander vitreus) dependent on body lipid reserves? A mulitpopulation comparative analysis. Can J Fish Aquat Sci 65:600–614
Morrill JC, Bales RC, Conkiln MH (2005) Estimating stream temperature from air temperature: implications for future water quality. J Environ Eng 131(1):139–146
Muth KM, Ickes BS (1993) Walleyes in Western Lake Erie, 1966 and 1990–1991. J Great Lakes Res 19:715–719
Pankhurst NW, Porter MJR (2003) Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physio Biochem 28:385–389
Plaza G, Sakaji H, Honda H, Hirota Y, Nashida K (2007) Spawning pattern and type of fecundity in relation to ovarian allometry in the round herring Etrumeus teres. Mar Biol 152:1051–1064
Pothoven SA, Nalepa TF, Schneeberger PJ, Brandt SB (2011) Changes in diet and body condition of Lake whitefish in southern Lake Michigan associated with changes in benthos. N Am J Fish Manage 21:876–883
Prowse T, Furgal C, Chouinard R, Melling H, Miburn D, Smith S (2009) Implications of climate change for economic development in northern Canada: energy and transportation sectors. AMBIO 38:272–281
Quintana L, Silva A, Berois N, Macadar O (2004) Temperature induces gonadal maturation and affects electrophysiological sexual maturity indicators in Brachyhypopomus pinnicaudatus from a temperate climate. J Exp Biol 207(11):1843–1853
Quist MC, Guy CS, Bernot RJ, Stephen JL (2002) Seasonal variation in condition, growth and food habits of walleye in a Great Plains reservoir and simulated effects of an altered thermal regime. J Fish Biol 61:1329–1344
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL https://www.R-project.org/
Reist JD, Swatzky CD, Johnson L (2016) The Arctic “great” lakes of Canada and their fish faunas-an overview in the context of Arctic change. J Great Lakes Res 42(2):173–192
Rieman B, Clayton J (2011) Wildfire and native fish: issues of forest health and conservation of sensitive species. Fisheries 22:6–15
Rinchard J, Dabrowski K, Ottobre J (2001) Sex steroids in plasma of lake whitefish Coregonus clupeaformis during spawning in Lake Erie. Comp Biochem Phys C 129:65–74
Roberge MM, Low G, Read CJ (1988) An assessment of the commercial fishery and population structure of walleye in Tathlina Lake, Northwest Territories. Can Tech Rep Fish Aquat Sci 1594: v + 54p
Roff DA (1983) An allocation model of growth and reproduction in fish. Can J Fish Aquat Sci 40:1395–1404
Rohatgi A (2019) WebPlotDigitizer. San Franscisco. URL: https://automeris.io/WebPlotDigitizer
Saborido-Rey F, Trippel E (2013) Fish reproduction and fisheries. Fish Res 138:1–4
Schindler DW, Smol JP (2006) Cumulative effects of climate warming and other human activities on freshwaters of arctic and subarctic North America. AMBIO 35:160–168
Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Bull Fish Res Board Can 184:966 p
Sharma S, Jackson DA, Minns CK, Shuter BJ (2007) Will northern fish populations be in hot water because of climate change? Glob Chang Biol 13:2052–2064
Sheppard K (2013) Spatial and seasonal variation in diet, growth and condition of walleye (Sander vitreus), sauger (Sander canadensis) and dwarf walleye (Sander vitreus) in Lake Winnipeg. Dissertation. University of Manitoba, Winnipeg
Sheppard KT, Hann BJ, Davoren GK (2018) Growth rate and condition of walleye (Sander vitreus), sauger (Sander canadensis), and dwarf walleye in a large Canadian lake. Can J Zool 96(7):739–747
Smol JP (2016) Arctic and Sub-Arctic shallow lakes in a multiple-stressor world: a paleoecological perspective. Hydrobiologia 778(1):253–272
Stewart DB, Low G (2000) A review of information on fish stocks and harvests in the Deh Cho area, Northwest Territories. Canadian Manuscript Report of Fisheries and Aquatic Sciences 2549: iv + 73 p
Stewart EM, Coleman KA, Korosi JB, Thienpont JR, Palmer MJ, Blais JM, Smol JP (2016) Assessing environmental stressors on commercial walleye fishery from a large northern ecosystem (Tathlina Lake) using water chemistry and paleolimnology. J Great Lakes Res 42(2):217–222
Thorsen A, Kjesbu OS (2001) A rapid method for estimation of oocyte size and potential fecundity in Atlantic cod using a computer-aided particle analysis system. J Sea Res 46:295–308
Van der Kraak G, Pankhurst NW (1997) Temperature effects on the reproductive performance of fish. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 159–176
Van der Oost R, Beyer J, Vermeulen N (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Phar 13:57–149
Wahl B, Loffler H (2009) Influences on the natural reproduction of whitefish (Coregonus lavaretus) in Lake Constance. Can J Fish Aquat Sci 66:547–556
Wootton RJ (1998) Ecology of teleost fishes, 2nd edn. Kluwer Academic Publishers, Dordrecht
Worm B, Hilborn R, Baum JK, Branch TA, Collie JS, Costello C, Fogarty MJ, Fulton EA, Hutchings JA, Jennings S, Jensen OP, Lotze H, Mace PM, McClanahan TR, Minto C, Palumbi SR, Parma AM, Ricard D, Rosenberg AA, Watson R, Zeller D (2009) Rebuilding global fisheries. Science 325:578–585
Wu RSS, Zhou BS, Randall DJ, Woo NYS, Lam PKS (2003) Aquatic hypoxia is an endocrine disruptor and impairs fish reproduction. Environ Sci Technol 37:1137–1141
Acknowledgements
The authors would like to acknowledge those who provided laboratory and field assistance, particularly members of the KTFN, including F. Simba, C. Chicot, D. Simba, T. Chicot, and notably M. Simba, as well as research technicians and associates from Wilfrid Laurier University (L. Jones, B. Pomeroy), the University of Waterloo/Environment Canada and Climate Change (G. Tetreault), the Dehcho Aboriginal Aquatic Resource and Oceans Management Program (AAROM) (M. Low, G. Low), and the Government of the Northwest Territories (M. Palmer, P. Cott). Funding for this study came from The Cumulative Impacts Monitoring Program (CIMP), The Northern Contaminants Program (NCP), and Wilfrid Laurier University. This project benefited from its collegial participation in the GNWT-Laurier (2008–2018) agreement to further community-based environmental research in the Northwest Territories. Grant Harrison was funded by a Natural Sciences and Engineering Research Council Collaborative Research and Training Experience (NSERC CREATE) grant awarded to the Canadian Rivers Institute at the University of New Brunswick (Co-I, D. MacLatchy).
Funding
Funding for this study came from The Cumulative Impacts Monitoring Program (CIMP), The Northern Contaminants Program (NCP), and Wilfrid Laurier University. This project benefited from its collegial participation in the GNWT-Laurier (2008–2018) agreement to further community-based environmental research in the Northwest Territories. Grant Harrison was funded by a Natural Sciences and Engineering Research Council Collaborative Research and Training Experience (NSERC CREATE) grant awarded to the Canadian Rivers Institute at the University of New Brunswick (Co-I, D. MacLatchy).
Author information
Authors and Affiliations
Contributions
Conceived and designed the investigation: D.L.M. and A.L.L., performed fieldwork and/or laboratory work: A.L.L. and G.H., contributed materials, reagents, and/or analysis tools: A.L.L. and D.L.M., analysed the data: H.J.D., wrote the paper: H.J.D., G.H., A.L.L. and D.L.M.
Corresponding author
Ethics declarations
Conflicts of interest/competing interests
The authors declare that they have no conflict of interest.
Ethics approval
An Animal Use Protocol was developed for this project, and approved by Wilfrid Laurier University’s Animal Care Committee.
Consent to participate
N/A
Consent for publication
N/A
Code availability
N/A
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 34 kb)
Rights and permissions
About this article
Cite this article
Dixon, H.J., Harrison, G., Lister, A.L. et al. Reproductive status of walleye (Sander vitreus) and lake whitefish (Coregonus clupeaformis) in two large, shallow Canadian subarctic lakes. Environ Biol Fish 103, 1119–1136 (2020). https://doi.org/10.1007/s10641-020-01010-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-020-01010-6