Winter is not coming: evaluating impacts of changing winter conditions on coregonine reproductive phenology

Special issue - Biology and Management of Coregonid Fishes - 2023

Open Access

Issue		Int. J. Lim. Volume 60, 2024 Special issue - Biology and Management of Coregonid Fishes - 2023


Article Number		17
Number of page(s)		16
DOI		https://doi.org/10.1051/limn/2024014
Published online		09 September 2024

Anneville O, Lainé L, Benker S, Ponticelli A, Gerdeaux D. 2007. Food habits and ontogentic changes in the diet of whitefish larvae in Lake Annecy. Bull Fr Pêche Piscic 21–33. [CrossRef] [EDP Sciences] [Google Scholar]
Anneville O, Lasne E, Guillard J, Eckmann R, Stockwell JD, Gillet C, Yule DL. 2015. Impact of fishing and stocking practices on coregonid diversity. Food Nutr Sci 06: 1045–1055. [Google Scholar]
Bhagowati B, Ahamad KU. 2019. A review on lake eutrophication dynamics and recent developments in lake modeling. Ecohydrol Hydrobiol 19: 155–166. [CrossRef] [Google Scholar]
Bogue MB. 2001. Fishing the Great Lakes: An Environmental History, 1783–1933. Madison, Wisconsin: Univ of Wisconsin Press. [Google Scholar]
Bourinet F, Anneville O, Drouineau H, Goulon C, Guillard J, Richard A. 2023. Synchrony in whitefish stock dynamics: disentangling the effects of local drivers and climate. J Limnol 82. [Google Scholar]
Bronte CR, Bunnell DB, David SR, Gordon R, Gorsky D, Millard MJ, Read J, Stein RA, Vaccaro L. 2017. Report from the workshop on coregonine restoration science. U.S. Geological Survey Open-File Report 2017-1081, 23 p, https://doi.org/10.3133/ofr20171081 [Google Scholar]
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB. 2004. Toward a metabolic theory of ecology. Ecology 85: 1771–1789. [CrossRef] [Google Scholar]
Burt JM, Hinch SG, Patterson DA. 2011. The importance of parentage in assessing temperature effects on fish early life history: a review of the experimental literature. Rev Fish Biol Fish 21: 377–406. [CrossRef] [Google Scholar]
Carpenter SR, Stanley EH, Vander Zanden MJ. 2011. State of the world's freshwater ecosystems: physical, chemical, and biological changes. Annu Rev Environ Resour 36: 75–99. [CrossRef] [Google Scholar]
Cline TJ, Bennington V, Kitchell JF. 2013. Climate change expands the spatial extent and duration of preferred thermal habitat for lake superior fishes. PLoS ONE 8: 1–8. [Google Scholar]
Colby PJ, Brooke LT. 1973. Effects of temperature on embryonic-development of lake herring (Coregonus artedii). J Fish Res Board Can 30: 799–810. [CrossRef] [Google Scholar]
Cushing DH. 1990. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26: 249–293. [CrossRef] [Google Scholar]
Dahlke FT, Wohlrab S, Butzin M, Pörtner H-O. 2020. Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science 369: 65–70. [CrossRef] [PubMed] [Google Scholar]
Desgué-Itier O, Melo Vieira Soares L, Anneville O, Bouffard D, Chanudet V, Danis PA, Domaizon I, Guillard J, Mazure T, Sharaf N, Soulignac F, Tran-Khac V, et al., 2023. Past and future climate change effects on the thermal regime and oxygen solubility of four peri-alpine lakes. Hydrol Earth Syst Sci 27: 837–859. [CrossRef] [Google Scholar]
DeWeber JT, Baer J, Rösch R, Brinker A. 2022. Turning summer into winter: nutrient dynamics, temperature, density dependence and invasive species drive bioenergetic processes and growth of a keystone coldwater fish. Oikos 2022: e09316. [CrossRef] [Google Scholar]
Eckmann R. 1987. A comparative study on the temperature dependence of embryogenesis in three coregonids (Coregonus spp.) from Lake Constance. Swiss J Hydrol 49: 353–362. [CrossRef] [Google Scholar]
Eronen T, Lahti E. 1988. Life cycle of winter spawning vendace (Coregonus albula L.) in Lake Kajoonjärvi, eastern Finland. Finn Fish Res 9: 197–203. [Google Scholar]
Eshenroder RL, Vecsei P, Gorman OT, Yule DL, Pratt TC, Mandrak NE, Bunnell DB, Muir AM. 2016. Ciscoes (Coregonus, subgenus Leucichthys) of the Laurentian Great Lakes and Lake Nipigon. Gt. Lakes Fish. Comm. Misc. Publ. 1: 156. [Google Scholar]
Farmer TM, Marschall EA, Dabrowski K, Ludsin SA. 2015. Short winters threaten temperate fish populations. Nat Commun 6: 7724. [CrossRef] [PubMed] [Google Scholar]
Gaudard A, Råman Vinnå L, Bärenbold F, Schmid M, Bouffard D. 2019. Toward an open access to high-frequency lake modeling and statistics data for scientists and practitioners-the case of Swiss lakes using Simstrat v2. 1. Geosci Model Dev 12: 3955–3974. [CrossRef] [Google Scholar]
Gillet C. 1989. Le déroulement de la fraie des principauxpoissons lacustres. Hydroécologie Appliquée 1: 117-143. [CrossRef] [EDP Sciences] [Google Scholar]
Gillooly JF, Charnov EL, West GB, Savage VM, Brown JH. 2002. Effects of size and temperature on developmental time. Nature 417: 70–73. [CrossRef] [PubMed] [Google Scholar]
Guzzo MM, Blanchfield PJ, Rennie MD. 2017. Behavioral responses to annual temperature variation alter the dominant energy pathway, growth, and condition of a cold-water predator. Proc Natl Acad Sci 114: 9912–9917. [CrossRef] [PubMed] [Google Scholar]
Hénault M, Fortin R. 1991. Early life stages, growth, and reproduction of spring-spawning ciscoes (Coregonus artedii) in Lac des Écorces, Quebec. Can J Zool 69: 1644–1652. [CrossRef] [Google Scholar]
Hjort J. 1914. Fluctuations in the great fisheries of Northern Europe. Copenhagen. [Google Scholar]
Hodgson EE, Hovel RA, Ward EJ, Lord S, Moore JW. 2020. Migratory diversity in an Arctic fish supporting subsistence harvest. Biol Conserv 248: 108685. [CrossRef] [Google Scholar]
Houde ED. 1989. Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects. Fish Bull 87: 471–495. [Google Scholar]
Houde ED, Hoyt RD. 1987. Fish early life dynamics and recruitment variability. Trans Am Fish Soc. [Google Scholar]
Im J, Kong D, Ghil S. 2016. Effects of water temperature on gonad development in the cold-water fish, kumgang fat minnow Rhynchocypris kumgangensis. Cytologia (Tokyo) 81: 311–317. [CrossRef] [Google Scholar]
IPCC. 2014. Climate Change 2014: Synthesis Report. Geneva, Switzerland: IPCC; 151 pp. [Google Scholar]
Jane SF, Hansen GJ, Benjamin K, Leavitt PR, Mincer JL, North RL, Pilla RM, Stetler JT, Williamson CE, Woolway RI, Arvola L, Chandra S, et al., 2020. Environmental Data Initiative. [Google Scholar]
Jeppesen E, Mehner T, Winfield IJ, Kangur K, Sarvala J, Gerdeaux D, Rask M, Malmquist HJ, Holmgren K, Volta P, Romo S, Eckmann R, et al., 2012. Impacts of climate warming on the long-term dynamics of key fish species in 24 European lakes. Hydrobiologia 694: 1–39. [CrossRef] [Google Scholar]
Jørgensen C, Ernande B, Fiksen Ø, Dieckmann U. 2006. The logic of skipped spawning in fish. Can J Fish Aquat Sci 63: 200–211. [CrossRef] [Google Scholar]
Kamler E. 2008. Resource allocation in yolk-feeding fish. Rev Fish Biol Fish 18: 143. [CrossRef] [Google Scholar]
Kangur K, Ginter K, Kangur A, Kangur P, Möls T. 2020. How did the late 1980s climate regime shift affect temperature-sensitive fish population dynamics: case study of Vendace (Coregonus albula) in a large north-temperate lake. Water 12: 2694. [CrossRef] [Google Scholar]
Karjalainen J, Jokinen L, Keskinen T, Marjomäki TJ. 2016. Environmental and genetic effects on larval hatching time in two coregonids. Hydrobiologia 780: 135–143. [CrossRef] [Google Scholar]
Karjalainen J, Juntunen J, Keskinen T, Koljonen S, Nyholm K, Ropponen J, Sjövik R, Taskinen S, Marjomäki TJ. 2019. Dispersion of vendace eggs and larvae around potential nursery areas reveals their reproductive strategy. Freshw Biol 64: 843–855. [CrossRef] [Google Scholar]
Karjalainen J, Keskinen T, Pulkkanen M, Marjomäki TJ. 2015. Climate change alters the egg development dynamics in cold-water adapted coregonids. Environ Biol Fishes 98: 979–991. [CrossRef] [Google Scholar]
Karjalainen J, Marjomäki TJ. 2018. Communal pair spawning behaviour of vendace (Coregonus albula) in the dark. Ecol Freshw Fish 27: 542–548. [CrossRef] [Google Scholar]
Kekäläinen J, Oskoei P, Janhunen M, Koskinen H, Kortet R, Huuskonen H. 2018. Sperm pre-fertilization thermal environment shapes offspring phenotype and performance. J Exp Biol 221: 1–8. [Google Scholar]
Kelly S, Moore TN, de Eyto E, Dillane M, Goulon C, Guillard J, Lasne E, McGinnity P, Poole R, Winfield IJ. 2020. Warming winters threaten peripheral Arctic charr populations of Europe. Clim Change 1–20. [Google Scholar]
Lange S. 2019. Trend-preserving bias adjustment and statistical downscaling with ISIMIP3BASD (v1. 0). Geosci Model Dev 12: 3055-3070. [CrossRef] [Google Scholar]
Lenth RV. 2021. emmeans: Estimated Marginal Means, aka Least-Squares Means. https://cran.r-project.org/package=emmeans. [Google Scholar]
Leppi JC, Rinella DJ, Wipfli MS, Liljedahl AK, Seitz AC, Falke JA. 2023. Climate change risks to freshwater subsistence fisheries in Arctic Alaska: insights and uncertainty from broad whitefish Coregonus nasus. Fisheries 48: 295–306. [CrossRef] [Google Scholar]
Little AG, Loughland I, Seebacher F. 2020. What do warming waters mean for fish physiology and fisheries? J Fish Biol 97: 328–340. [CrossRef] [PubMed] [Google Scholar]
Lowerre-Barbieri SK, Ganias K, Saborido-Rey F, Murua H, Hunter JR. 2011. Reproductive timing in marine fishes: variability, temporal scales, and methods. Mar Coast Fish 3: 71–91. [CrossRef] [Google Scholar]
Lucke VS, Stewart TR, Vinson MR, Glase JD, Stockwell JD. 2020. Larval Coregonus spp. diets and zooplankton community patterns in the Apostle Islands, Lake Superior. J Gt Lakes Res 46: 1391–1401. [CrossRef] [Google Scholar]
Luczyński M, Kirklewska A. 1984. Dependence of Coregonus albula embryogenesis rate on the incubation temperature. Aquaculture 42: 43–55. [CrossRef] [Google Scholar]
Lynch AJ, Cooke SJ, Deines AM, Bower SD, Bunnell DB, Cowx IG, Nguyen VM, Nohner J, Phouthavong K, Riley B, Rogers MW, Taylor WW, et al., 2016. The social, economic, and environmental importance of inland fish and fisheries. Environ Rev 24: 115–121. [CrossRef] [Google Scholar]
Lyons J, Rypel AL, Rasmussen PW, Burzynski TE, Eggold BT, Myers JT, Paoli TJ, McIntyre PB. 2015. Trends in the reproductive phenology of two Great Lakes fishes. Trans Am Fish Soc 144: 1263–1274. [CrossRef] [Google Scholar]
Maberly SC, O'Donnell RA, Woolway RI, Cutler MEJ, Gong M, Jones ID, Merchant CJ, Miller CA, Politi E, Scott EM. 2020. Global lake thermal regions shift under climate change. Nat Commun 11: 1–9. [CrossRef] [PubMed] [Google Scholar]
Marjomäki TJ, Auvinen H, Helminen H, Huusko A, Sarvala J, Valkeajärvi P, Viljanen M, Karjalainen J. 2004. Spatial synchrony in the inter-annual population variation of vendace (Coregonus albula (L.)) in Finnish lakes. Ann Zool Fenn 41: 225–240. [Google Scholar]
McKenna JE, Stott W, Chalupnicki M, Johnson JH. 2020. Spatial segregation of cisco (Coregonus artedi) and lake whitefish (C. clupeaformis) larvae in Chaumont Bay, Lake Ontario. J Gt Lakes Res 46: 1485–1490. [CrossRef] [Google Scholar]
McQuinn IH. 1997. Metapopulations and the Atlantic Herring. Rev Fish Biol Fish 7: 297–329. [CrossRef] [Google Scholar]
Miller TJ, Crowder LB, Rice JA, Marschall EA. 1988. Larval size and recruitment mechanisms in fishes: toward a conceptual framework. Can J Fish Aquat Sci 45: 1657–1670. [CrossRef] [Google Scholar]
Muir AM, Vecsei P, Pratt TC, Krueger CC, Power M, Reist JD. 2013. Ontogenetic shifts in morphology and resource use of cisco Coregonus artedi. J Fish Biol 82: 600–617. [CrossRef] [PubMed] [Google Scholar]
Myers JT, Yule DL, Jones ML, Quinlan HR, Berglund EK. 2014. Foraging and predation risk for larval cisco (Coregonus artedi) in Lake Superior: a modelling synthesis of empirical survey data. Ecol Model 294: 71–83. [CrossRef] [Google Scholar]
Nagahama Y, Yamashita M. 2008. Regulation of oocyte maturation in fish. Dev Growth Differ 50: S195–S219. [CrossRef] [PubMed] [Google Scholar]
Nyberg P, Bergstrand E, Degerman E, Enderlein O. 2001. Recruitment of pelagic fish in an unstable climate: studies in Sweden's four largest lakes. Ambio 30: 559–564. [CrossRef] [PubMed] [Google Scholar]
Ohlberger J, Mehner T, Staaks G, Hölker F. 2008. Is ecological segregation in a pair of sympatric coregonines supported by divergent feeding efficiencies? Can J Fish Aquat Sci 65: 2105–2113. [CrossRef] [Google Scholar]
O'Reilly CM, Rowley RJ, Schneider P, Lenters JD, Mcintyre PB, Kraemer BM. 2015. Rapid and highly variable warming of lake surface waters around the globe. Geophys Res Lett 42: 1–9. [Google Scholar]
Oyadomari JK, Auer NN. 2007. Influence of rearing temperature and feeding regime on Otolith increment deposition in larval Ciscoes. Trans Am Fish Soc 136: 766–777. [CrossRef] [Google Scholar]
Parks TP, Rypel AL. 2018. Predator-prey dynamics mediate long-term production trends of cisco (Coregonus artedi) in a northern Wisconsin lake. Can J Fish Aquat Sci 75: 1969–1976. [CrossRef] [Google Scholar]
Parmesan C. 2006. Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37: 637–669. [CrossRef] [Google Scholar]
Perrier C, Molinero JC, Gerdeaux D, Anneville O. 2012. Effects of temperature and food supply on the growth of whitefish Coregonus lavaretus larvae in an oligotrophic peri-alpine lake. J Fish Biol 81: 1501–1513. [CrossRef] [PubMed] [Google Scholar]
R Core Team, 2023. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, https://www.r-project.org/. [Google Scholar]
Reist JD, Wrona FJ, Prowse TD, Power M, Dempson JB, Beamish RJ, King JR, Carmichael TJ, Sawatzky CD. 2006. General effects of climate change on Arctic fishes and fish populations. AMBIO J Hum Environ 35: 370–380. [CrossRef] [PubMed] [Google Scholar]
Schulz M, Freyhof J, Saint-Laurent R, Østbye K, Mehner T, Bernatchez L. 2006. Evidence for independent origin of two spring-spawning ciscoes (Salmoniformes: Coregonidae) in Germany. J Fish Biol 68: 119–135. [CrossRef] [Google Scholar]
Sharma S, Blagrave K, Magnuson JJ, O'Reilly CM, Oliver S, Batt RD, Magee MR, Straile D, Weyhenmeyer GA, Winslow LA. 2019. Widespread loss of lake ice around the Northern Hemisphere in a warming world. Nat Clim Change 9: 227. [CrossRef] [Google Scholar]
Slesinger E, Jensen OP, Saba G. 2021. Spawning phenology of a rapidly shifting marine fish species throughout its range. ICES J Mar Sci 78: 1010–1022. [CrossRef] [Google Scholar]
Sommer U, Adrian R, De Senerpont Domis L, Elser JJ, Gaedke U, Ibelings B, Jeppesen E, Lürling M, Molinero JC, Mooij WM. 2012. Beyond the Plankton Ecology Group (PEG) model: mechanisms driving plankton succession. Annu Rev Ecol Evol Syst 43: 429–448. [CrossRef] [Google Scholar]
Stewart TR, Brun C, Goulon C, Baer J, Karjalainen J, Guillard J, Lasne E. in review. Response of whitefish embryos to thermal conditions diverges between perialpine populations. Int J Limnol. DOI: https://doi.org/10.1051/limn/2024017 [Google Scholar]
Stewart TR, Mäkinen M, Goulon C, Guillard J, Marjomäki TJ, Lasne E, Karjalainen J, Stockwell JD. 2021a. Influence of warming temperatures on coregonine embryogenesis within and among species. Hydrobiologia 848: 4363–4385. [CrossRef] [Google Scholar]
Stewart TR, Vinson MR, Stockwell JD. 2021b. Shining a light on Laurentian Great Lakes cisco (Coregonus artedi): how ice coverage may impact embryonic development. J Gt Lakes Res 47: 1410–1418. [CrossRef] [Google Scholar]
Stockwell JD, Yule DL, Hrabik TR, Sierszen ME, Isaac EJ. 2014. Habitat coupling in a large lake system: delivery of an energy subsidy by an offshore planktivore to the nearshore zone of Lake Superior. Freshw Biol 59: 1197-1212. [CrossRef] [Google Scholar]
Straile D, Eckmann R, Jüngling T, Thomas G, Löffler H. 2007. Influence of climate variability on whitefish (Coregonus lavaretus) year-class strength in a deep, warm monomictic lake. Oecologia 151: 521–529. [CrossRef] [PubMed] [Google Scholar]
Straile D, Kerimoglu O, Peeters F. 2015. Trophic mismatch requires seasonal heterogeneity of warming. Ecology 96: 2794–2805. [CrossRef] [PubMed] [Google Scholar]
Tunney TD, McCann KS, Lester NP, Shuter BJ. 2014. Effects of differential habitat warming on complex communities. Proc Natl Acad Sci 111: 8077–8082. [CrossRef] [PubMed] [Google Scholar]
U.S. Geological Survey, 2024, USGS 04249000, Oswego River at Lock 7, Oswego, NY, in USGS water data for the Nation: U.S. Geological Survey National Water Information System database, accessed 14 September 2021 at https://doi.org/10.5066/F7P55KJN. [Site information directly accessible at https://waterdata.usgs.gov/nwis/uv?site_no=04249000&legacy=1] [Google Scholar]
Vinson MR, Herbert ME, Ackiss AS, Dobosenski JA, Evrard LM, Gorman OT, Lyons JF, Phillips SB, Yule DL. 2023. Lake Superior Kiyi reproductive biology. Trans Am Fish Soc 152: 75–93. [CrossRef] [Google Scholar]
Volta P, Jeppesen E, Sala P, Galafassi S, Foglini C, Puzzi C, Winfield IJ. 2018. Fish assemblages in deep Italian subalpine lakes: history and present status with an emphasis on non-native species. Hydrobiologia 824: 255–270. [CrossRef] [Google Scholar]
Warszawski L, Frieler K, Huber V, Piontek F, Serdeczny O, Schewe J. 2014. The inter-sectoral impact model intercomparison project (ISI-MIP): project framework. Proc Natl Acad Sci 111:3228–3232. [CrossRef] [PubMed] [Google Scholar]
Winder M, Schindler DE. 2004. Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85: 2100–2106. [CrossRef] [Google Scholar]
Winslow LA, Read JS, Hansen GJA, Rose KC, Robertson DM. 2017. Seasonality of change: summer warming rates do not fully represent effects of climate change on lake temperatures. Limnol Oceanogr 62: 2168–2178. [CrossRef] [Google Scholar]
Woods T, Kaz A, Giam X. 2021. Phenology in freshwaters: a review and recommendations for future research. Ecography 44: 1–14. [CrossRef] [Google Scholar]
Woolway RI. 2023. The pace of shifting seasons in lakes. Nat Commun 14: 2101. [CrossRef] [PubMed] [Google Scholar]
Woolway RI, Sharma S, Weyhenmeyer GA, Debolskiy A, Golub M, Mercado-Bettín D, Perroud M, Stepanenko V, Tan Z, Grant L. 2021. Phenological shifts in lake stratification under climate change. Nat Commun 12: 1–11. [CrossRef] [PubMed] [Google Scholar]
Yankova Y, Neuenschwander S, Köster O, Posch T. 2017. Abrupt stop of deep water turnover with lake warming: drastic consequences for algal primary producers. Sci Rep 7: 1–9. [CrossRef] [PubMed] [Google Scholar]
Yule DL, Stockwell JD, Black JA, Cullis KI, Cholwek GA, Myers JT. 2008. How systematic age underestimation can impede understanding of fish population dynamics: lessons learned from a lake superior Cisco Stock. Trans Am Fish Soc 137: 481–495. [CrossRef] [Google Scholar]
Zeller D, Booth S, Pakhomov E, Swartz W, Pauly D. 2011. Arctic fisheries catches in Russia, USA, and Canada: baselines for neglected ecosystems. Polar Biol 34: 955–973. [CrossRef] [Google Scholar]
Zimmerman MS, Krueger CC. 2009. An ecosystem perspective on re-establishing native deepwater fishes in the Laurentian Great Lakes. North Am J Fish Manag 29: 1352–1371. [CrossRef] [Google Scholar]

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.