Skip to main content

Advertisement

Log in

Influence of warming temperatures on coregonine embryogenesis within and among species

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The greatest known global response of lakes to climate change has been an increase in water temperatures. The responses of many lake fishes to warming water temperatures are projected to be inadequate to counter the speed and magnitude of climate change. We experimentally evaluated the responses of embryos from a group of cold, stenothermic fishes (Salmonidae Coregoninae) to increased incubation temperatures. Study groups included cisco (Coregonus artedi) from lakes Superior and Ontario (USA), and vendace (C. albula) and European whitefish (C. lavaretus) from Lake Southern Konnevesi (Finland). Embryos from artificial crossings were incubated at water temperatures of 2.0, 4.5, 7.0, and 9.0°C, and their responses were quantified for developmental and morphological traits. Embryo survival, incubation period, and length-at-hatch were inversely related to incubation temperature whereas yolk-sac volume increased with incubation temperature within study groups. However, varying magnitudes of responses among study groups suggested differential levels of developmental plasticity to climate change. Differential levels of parental effects indicate genetic diversity may enable all study groups to adapt to cope with some degree of changing environmental conditions. Our results suggest that the coregonines sampled within and among systems may have a wide range of embryo responses to warming incubation conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of data and material

The datasets generated during and/or analyzed during the current study are available in the GitHub repository, https://github.com/taylorstewart/Stewart-et-al-2021---Coregonine-Temp-Embryo.

Code availability

The scripts to reproduce the figures and analyses in this paper are available in the GitHub repository, https://github.com/taylorstewart/Stewart-et-al-2021---Coregonine-Temp-Embryo.

References

  • Anneville, O., E. Lasne, J. Guillard, R. Eckmann, J. D. Stockwell, C. Gillet & D. L. Yule, 2015. Impact of fishing and stocking practices on Coregonid diversity. Food and Nutrition Sciences 06: 1045–1055.

    Article  Google Scholar 

  • Austin, J. A. & S. M. Colman, 2007. Lake Superior summer water temperatures are increasing more rapidly than regional temperatures: a positive ice-albedo feedback. Geophysical Research Letters 34: 1–5.

    Article  Google Scholar 

  • Bates, D., M. Mächler, B. Bolker & S. Walker, 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.

    Article  Google Scholar 

  • Billerbeck, J. M., E. T. Schultz & D. O. Conover, 2000. Adaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside. Oecologia 122: 210–219.

    Article  CAS  PubMed  Google Scholar 

  • Blaxter, J. H. S., 1991. The effect of temperature on larval fishes. Netherlands Journal of Zoology 42: 336–357.

    Article  Google Scholar 

  • Blaxter, J. H. S. & G. Hempel, 1963. The influence of egg size on herring larvae (Clupea harengus L.). Journal du Conseil/Conseil Permanent International pour l’Exploration de la Mer 28: 211–240.

    Article  Google Scholar 

  • Brett, J. R., 1979. Environmental Factors and Growth In Hoar, W. S., D. J. Randall, & J. R. Brett (eds), Fish Physiology. Elsevier Science: 599–677.

  • Bronte, C. R., D. B. Bunnell, S. R. David, R. Gordon, D. Gorsky, M. J. Millard, J. Read, R. A. Stein, & L. Vaccaro, 2017. Report from the workshop on coregonine restoration science. US Geological Survey.

  • Brooke, L. T. & P. J. Colby, 1980. Development and survival of embryos of lake herring at different constant oxygen concentrations and temperatures. The Progressive Fish-Culturist 42: 3–9.

    Article  Google Scholar 

  • Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage & G. B. West, 2004. Toward a metabolic theory of ecology. Ecology 85: 1771–1789.

    Article  Google Scholar 

  • Busch, S., G. Kirillin & T. Mehner, 2012. Plasticity in habitat use determines metabolic response of fish to global warming in stratified lakes. Oecologia 170: 275–287.

    Article  PubMed  Google Scholar 

  • Chavarie, L., J. B. Dempson, C. J. Schwarz, J. D. Reist, G. Power & M. Power, 2010. Latitudinal variation in growth among Arctic charr in eastern North America: evidence for countergradient variation? Hydrobiologia 650: 161–177.

    Article  Google Scholar 

  • Chen, Z., A. P. Farrell, A. Matala & S. R. Narum, 2018. Mechanisms of thermal adaptation and evolutionary potential of conspecific populations to changing environments. Molecular Ecology 27: 659–674.

    Article  PubMed  Google Scholar 

  • Christensen, J. H., B. Hewitson, A. Busuioc, A. Chen, X. Gao, I. Held, R. Jones, R. K. Kolli, W. T. Kwon, R. Laprise, V. Magana Rueda, L. Mearns, C. G. Menendez, J. Raisanen, A. Rinke, A. Sarr, & P. Whetton, 2007. Regional Climate Projections. Chapter 11. Cambridge University Press, Cambridge (United Kingdom), United Kingdom.

  • Christie, M. R., M. L. Marine, R. A. French & M. S. Blouin, 2012. Genetic adaptation to captivity can occur in a single generation. Proceedings of the National Academy of Sciences 109: 238–242.

    Article  CAS  Google Scholar 

  • Cline, T. J., V. Bennington, J. F. Kitchell, C. Fulton. (2013) Climate change expands the spatial extent and duration of preferred thermal habitat for Lake Superior fishes. PLoS ONE 8(4): e62279.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colby, P. J., & L. T. Brooke, 1970. Survival and development of lake herring (Coregonus artedii) eggs at various incubation temperatures. Biology of Coregonid Fishes 417–428.

  • Colby, P. J. & L. T. Brooke, 1973. Effects of temperature on embryonic-development of Lake Herring (Coregonus artedii). Journal of the Fisheries Research Board of Canada 30: 799–810.

    Article  Google Scholar 

  • Comte, L., L. Buisson, M. Daufresne & G. Grenouillet, 2013. Climate-induced changes in the distribution of freshwater fish: observed and predicted trends. Freshwater Biology 58: 625–639.

    Article  Google Scholar 

  • Conover, D. O. & M. C. Present, 1990. Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologica 83: 316–324.

    Article  Google Scholar 

  • Conover, D. O. & E. T. Schultz, 1995. Phenotypic similarity and the evolutionary significance of countergradient variation. Trends in Ecology & Evolution 10: 248–252.

    Article  CAS  Google Scholar 

  • Cushing, D. H., 1990. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Advances in Marine Biology 26: 249–293.

    Article  Google Scholar 

  • Dahlke, F. T., S. Wohlrab, M. Butzin & H.-O. Pörtner, 2020. Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science 369: 65–70.

    Article  CAS  PubMed  Google Scholar 

  • Dryer, W. R. & J. Beil, 1964. Life history of lake herring in Lake Superior. Fish. Bull 63: 493–530.

    Google Scholar 

  • Ebener, M. P., J. D. Stockwell, D. L. Yule, O. T. Gorman, T. R. Hrabik, R. E. Kinnunen, W. P. Mattes, J. K. Oyadomari, D. R. Schreiner, S. Geving, K. Scribner, S. T. Schram, M. J. Seider & S. P. Sitar, 2008. Status of cisco (Coregonus artedi) in Lake Superior during 1970-2006 and management and research considerations. Ann Arbor, Michigan: Great Lakes Fishery Commission, Lake Superior Technical Report 1: 126.

    Google Scholar 

  • Edsall, T. A. & P. J. Colby, 1970. Temperature tolerance of young-of-the-year cisco, Coregonus artedii. Transactions of the American Fisheries Society 99: 526–531.

    Article  Google Scholar 

  • Elliott, J. A. & V. A. Bell, 2011. Predicting the potential long-term influence of climate change on vendace (Coregonus albula) habitat in Bassenthwaite Lake, U.K. Freshwater Biology 56: 395–405.

    Article  Google Scholar 

  • Eronen, T. & E. Lahti, 1988. Life cycle of winter spawning vendace (Coregonus albula L.) in Lake Kajoonjärvi, eastern Finland. Finnish Fisheries Research 9: 197–203.

    Google Scholar 

  • Eshenroder, R. L., P. Vecsei, O. T. Gorman, D. L. Yule, T. C. Pratt, N. E. Mandrak, D. B. Bunnell, & A. M. Muir, 2016. Ciscoes (Coregonus, subgenus Leucichthys) of the Laurentian Great Lakes and Lake Nipigon. Canadian Journal of Fisheries and Aquatic Sciences. Great Lakes Fishery Commission.

  • Favé, M.-J. & J. Turgeon, 2008. Patterns of genetic diversity in Great Lakes bloaters (Coregonus hoyi) with a view to future reintroduction in Lake Ontario. Conservation Genetics 9: 281–293.

    Article  Google Scholar 

  • Ficke, A. D., C. A. Myrick & L. J. Hansen, 2007. Potential impacts of global climate change on freshwater fisheries. Reviews in Fish Biology and Fisheries 17: 581–613.

    Article  Google Scholar 

  • Figge, F., 2004. Bio-folio: applying portfolio theory to biodiversity. Biodiversity & Conservation 13: 827–849.

    Article  Google Scholar 

  • Ford, M. J., 2002. Selection in captivity during supportive breeding may reduce fitness in the wild. Conservation Biology 16: 815–825.

    Article  Google Scholar 

  • Fox, R. J., J. M. Donelson, C. Schunter, T. Ravasi & J. D. Gaitán-Espitia, 2019. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philosophical Transactions of the Royal Society B: Biological Sciences 374: 1–9.

    Article  Google Scholar 

  • Freshwater, C., S. C. Anderson, K. R. Holt, A. Huang & C. A. Holt, 2019. Weakened portfolio effects constrain management effectiveness for population aggregates. Ecological Applications 29: 1–14.

    Article  Google Scholar 

  • Fry, F. E. J. 1964. Animals in aquatic environments: fishes. Handbook of physiology Williams and Wilkins Baltimore 4: 715–728.

  • Garland, T., A. F. Bennett & E. L. Rezende, 2005. Phylogenetic approaches in comparative physiology. Journal of Experimental Biology 208: 3015–3035.

    Article  PubMed  Google Scholar 

  • Gillooly, J. F., E. L. Charnov, G. B. West, V. M. Savage & J. H. Brown, 2002. Effects of size and temperature on developmental time. Nature 417: 70–73.

    Article  CAS  PubMed  Google Scholar 

  • Häkkinen, J., E. Vehniäinen, O. Ylönen, J. J. Heikkilä, M. Soimasuo, J. Kaurola, A. Oikari & J. Karjalainen, 2002. The effects of increasing UV-B radiation on pigmentation, growth and survival of coregonid embryos and larvae. Environmental Biology of Fishes 64: 451–459.

    Article  Google Scholar 

  • Halpern, B. S., M. Frazier, J. Potapenko, K. S. Casey, K. Koenig, C. Longo, J. S. Lowndes, R. C. Rockwood, E. R. Selig, K. A. Selkoe & S. Walbridge, 2015. Spatial and temporal changes in cumulative human impacts on the world’s ocean. Nature Communications 6: 1–7.

    Article  CAS  Google Scholar 

  • Hansen, G. J. A., J. S. Read, J. F. Hansen & L. A. Winslow, 2017. Projected shifts in fish species dominance in Wisconsin lakes under climate change. Global Change Biology 23: 1463–1476.

    Article  PubMed  Google Scholar 

  • Heikkilä, J. J., H. Huuskonen & J. Karjalainen, 2006. Location of spawning grounds of vendace (Coregonus albula (L.)): implication for dispersion of newly hatched larvae. Internationale Vereinigung für theoretische und angewandte Limnologie: Verhandlungen 29: 1725–1728.

    Google Scholar 

  • Hénault, M. & R. Fortin, 1989. Comparison of meristic and morphometric characters among spring-and fall-spawning ecotypes of cisco (Coregonus artedii) in southern Quebec, Canada. Canadian Journal of Fisheries and Aquatic Sciences 46: 166–173.

    Article  Google Scholar 

  • Hénault, M. & R. Fortin, 1991. Early life stages, growth, and reproduction of spring-spawning ciscoes (Coregonus artedii) in Lac des Écorces, Quebec. Canadian Journal of Zoology 69: 1644–1652.

    Article  Google Scholar 

  • Herb, W. R., L. B. Johnson, P. C. Jacobson & H. G. Stefan, 2014. Projecting cold-water fish habitat in lakes of the glacial lakes region under changing land use and climate regimes. Canadian Journal of Fisheries and Aquatic Sciences 71: 1334–1348.

    Article  CAS  Google Scholar 

  • Hodson, P. V. & B. R. Blunt, 1986. The effect of time from hatch on the yolk conversion efficiency of rainbow trout, Salmo gairdneri. Journal of Fish Biology 29: 37–46.

    Article  Google Scholar 

  • Hoffmann, A. A. & C. M. Sgrò, 2011. Climate change and evolutionary adaptation. Nature Australia 470: 479–485.

    Article  CAS  Google Scholar 

  • Houde, A. L. S. & T. E. Pitcher, 2016. fullfact: an R package for the analysis of genetic and maternal variance components from full factorial mating designs. Ecology and Evolution 6: 1656–1665.

    Article  PubMed  PubMed Central  Google Scholar 

  • Howells, E. J., D. Abrego, E. Meyer, N. L. Kirk & J. A. Burt, 2016. Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Global Change Biology 22: 2702–2714.

    Article  PubMed  Google Scholar 

  • Huuskonen, H., J. Kekäläinen, B. Panda, T. Shikano & R. Kortet, 2011. Embryonic survival and larval predator-avoidance ability in mutually ornamented whitefish. Biological Journal of the Linnean Society 103: 593–601.

    Article  Google Scholar 

  • Isaak, D. J., 2014. Climate change and the future of freshwater fisheries. In Taylor, W. W., A. J. Lynch, & N. J. Leonard (eds), Future of Fisheries: Perspectives for Emerging Professionals. American Fisheries Society, Bethesda, MD: 435–441.

  • ISO 6341, 2012. Water Quality — Determination of the inhibition of the mobility of Daphnia magna Straus (Cladocera, Crustacea) — Acute toxicity test. International Organization for Standardization, from https://www.iso.org/standard/54614.html.

  • Jacobson, P. C., H. G. Stefan & D. L. Pereira, 2010. Coldwater fish oxythermal habitat in Minnesota lakes: influence of total phosphorus, July air temperature, and relative depth. Canadian Journal of Fisheries and Aquatic Sciences 67: 2002–2013.

    Article  CAS  Google Scholar 

  • Jane, S. F., G. J. Hansen, K. Benjamin, P. R. Leavitt, J. L. Mincer, R. L. North, R. M. Pilla, J. T. Stetler, C. E. Williamson, R. Woolway, L. Arvola, S. Chandra, C. L. DeGasperi, L. Diemer, J. Dunalska, O. Erina, G. Flaim, H. Grossart, K. Hambright, C. Hein, J. Hejzlar, L. L. Janus, J. Jenny, J. R. Jones, L. B. Knoll, B. Leoni, E. Mackay, S. S. Matsuzaki, C. McBride, D. C. Mueller-Navarra, A. M. Paterson, D. Pierson, M. Rogora, J. A. Rusak, S. Sadro, E. Saulnier-Talbot, M. Schmid, R. Sommaruga, W. Thiery, P. Verburg, K.. Weathers, & K. C. Rose, 2020. Widespread deoxygenation of temperate lakes: companion dataset 1980 - 2017 ver 1. Environmental Data Initiative, https://doi.org/10.6073/pasta/ac8b05bb0da19032b3df3efc21f83874.

  • Jenny, J.-P., O. Anneville, F. Arnaud, Y. Baulaz, D. Bouffard, I. Domaizon, S. A. Bocaniov, N. Chèvre, M. Dittrich & J.-M. Dorioz, 2020. Scientists’ Warning to Humanity: rapid degradation of the world’s large lakes. Journal of Great Lakes Research 46: 686–702.

    Article  Google Scholar 

  • Jeppesen, E., T. Mehner, I. J. Winfield, K. Kangur, J. Sarvala, D. Gerdeaux, M. Rask, H. J. Malmquist, K. Holmgren, P. Volta, S. Romo, R. Eckmann, A. Sandström, S. Blanco, A. Kangur, H. Ragnarsson Stabo, M. Tarvainen, A. M. Ventelä, M. Søndergaard, T. L. Lauridsen & M. Meerhoff, 2012. Impacts of climate warming on the long-term dynamics of key fish species in 24 European lakes. Hydrobiologia 694: 1–39.

    Article  CAS  Google Scholar 

  • Jobling, M., 1981. Temperature tolerance and the final preferendum—rapid methods for the assessment of optimum growth temperatures. Journal of Fish Biology 19: 439–455.

    Article  Google Scholar 

  • Jonassen, T., 2000. Geographic variation in growth and food conversion efficiency of juvenile Atlantic halibut related to latitude. Journal of Fish Biology 56: 279–294.

    Article  Google Scholar 

  • Jonsson, B. & N. Jonsson, 2014. Early environment influences later performance in fishes. Journal of Fish Biology 85: 151–188.

    Article  CAS  PubMed  Google Scholar 

  • Jørgensen, C., B. Ernande, Ø. Fiksen & U. Dieckmann, 2006. The logic of skipped spawning in fish. Canadian Journal of Fisheries and Aquatic Sciences 63: 200–211.

    Article  Google Scholar 

  • Kamler, E., 2008. Resource allocation in yolk-feeding fish. Reviews in Fish Biology and Fisheries 18: 143–200.

    Article  Google Scholar 

  • Karjalainen, J., 1992. Effects of different preservation methods on total length and weight of larval vendace (Coregonus albula (L.)). Nordic Journal of Freshwater Research (Sweden) 67: 88–89.

    Google Scholar 

  • Karjalainen, J. & T. J. Marjomäki, 2018. Communal pair spawning behaviour of vendace (Coregonus albula) in the dark. Ecology of Freshwater Fish 27: 542–548.

    Article  Google Scholar 

  • Karjalainen, J., T. Keskinen, M. Pulkkanen & T. J. Marjomäki, 2015. Climate change alters the egg development dynamics in cold-water adapted coregonids. Environmental Biology of Fishes 98: 979–991.

    Article  Google Scholar 

  • Karjalainen, J., L. Jokinen, T. Keskinen & T. J. Marjomäki, 2016a. Environmental and genetic effects on larval hatching time in two coregonids. Hydrobiologia 780: 135–143.

    Article  Google Scholar 

  • Karjalainen, J., O. Urpanen, T. Keskinen, H. Huuskonen, J. Sarvala, P. Valkeajärvi & T. J. Marjomäki, 2016b. Phenotypic plasticity in growth and fecundity induced by strong population fluctuations affects reproductive traits of female fish. Ecology and Evolution 6: 779–790.

    Article  PubMed  PubMed Central  Google Scholar 

  • Karjalainen, J., M. Tuloisela, K. Nyholm, & T. J. Marjomäki, 2021. Vendace (Coregonus albula) disperse their eggs widely during spawning. Annales Zoologici Fennici 58: 141–153.

  • Kekäläinen, J., P. Oskoei, M. Janhunen, H. Koskinen, R. Kortet & H. Huuskonen, 2018. Sperm pre-fertilization thermal environment shapes offspring phenotype and performance. Journal of Experimental Biology 221: 1–8.

    Google Scholar 

  • Kennedy, J., A. J. Geffen & R. D. M. Nash, 2007. Maternal influences on egg and larval characteristics of plaice (Pleuronectes platessa L.). Journal of Sea Research 58: 65–77.

    Article  Google Scholar 

  • Langhans, S. D., S. C. Jähnig, M. Lago, A. Schmidt-Kloiber & T. Hein, 2019. The potential of ecosystem-based management to integrate biodiversity conservation and ecosystem service provision in aquatic ecosystems. Science of The Total Environment 672: 1017–1020.

    Article  CAS  PubMed  Google Scholar 

  • Lim, M. Y.-T., R. G. Manzon, C. M. Somers, D. R. Boreham & J. Y. Wilson, 2017. The effects of fluctuating temperature regimes on the embryonic development of lake whitefish (Coregonus clupeaformis). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 214: 19–29.

    Article  CAS  Google Scholar 

  • Little, A. G., I. Loughland & F. Seebacher, 2020. What do warming waters mean for fish physiology and fisheries? Journal of Fish Biology 97: 328–340.

    Article  CAS  PubMed  Google Scholar 

  • Luck, G. W., G. C. Daily & P. R. Ehrlich, 2003. Population diversity and ecosystem services. Trends in Ecology & Evolution 18: 331–336.

    Article  Google Scholar 

  • Luczynski, M. & A. Kirklewska, 1984. Dependence of Coregonus albula embryogenesis rate on the incubation temperature. Aquaculture 42: 43–55.

    Article  Google Scholar 

  • Lynch, A. J., W. W. Taylor, T. D. Beard & B. M. Lofgren, 2015. Climate change projections for lake whitefish (Coregonus clupeaformis) recruitment in the 1836 Treaty Waters of the Upper Great Lakes. Journal of Great Lakes Research 41: 415–422.

    Article  Google Scholar 

  • Lynch, A. J., S. J. Cooke, A. M. Deines, S. D. Bower, D. B. Bunnell, I. G. Cowx, V. M. Nguyen, J. Nohner, K. Phouthavong, B. Riley, M. W. Rogers, W. W. Taylor, W. Woelmer, S.-J. Youn & T. D. Beard, 2016. The social, economic, and environmental importance of inland fish and fisheries. Environmental Reviews 24: 115–121.

    Article  Google Scholar 

  • Luke, S. G. (2017) Evaluating significance in linear mixed-effects models in R. Behavior Research Methods 49(4): 1494-1502.

    Article  PubMed  Google Scholar 

  • Maberly, S. C., R. A. O’Donnell, R. I. Woolway, M. E. J. Cutler, M. Gong, I. D. Jones, C. J. Merchant, C. A. Miller, E. Politi & E. M. Scott, 2020. Global lake thermal regions shift under climate change. Nature Communications 11: 1–9.

    Article  CAS  Google Scholar 

  • Mari, L., L. Garaud, G. Evanno & E. Lasne, 2016. Higher temperature exacerbates the impact of sediments on embryo performances in a salmonid. Biology Letters 12: 20160745.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mari, L., M. Daufresne, J. Guillard, G. Evanno, & E. Lasne, 2021. Elevated temperature and deposited sediment jointly affect early life history traits in southernmost arctic charr populations. Canadian Journal of Fisheries and Aquatic Sciences 78: 744–751.

    Article  Google Scholar 

  • Marjomäki, T. J., H. Auvinen, H. Helminen, A. Huusko, J. Sarvala, P. Valkeajärvi, M. Viljanen & J. Karjalainen, 2004. Spatial synchrony in the inter-annual population variation of vendace (Coregonus albula (L.)) in Finnish lakes. Annales Zoologici Fennici 41: 225–240.

    Google Scholar 

  • McBride, R. S., S. Somarakis, G. R. Fitzhugh, A. Albert, N. A. Yaragina, M. J. Wuenschel, A. Alonso-Fernández & G. Basilone, 2015. Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish and Fisheries 16: 23–57.

    Article  Google Scholar 

  • McCormick, J. H., B. R. Jones & R. F. Syrett, 1971. Temperature requirements for growth and survival of larval ciscos (Coregonus artedii). Journal of the Fisheries Board of Canada 28: 924–927.

    Article  Google Scholar 

  • Mcphee, M. V., D. L. G. Noakes & F. W. Allendorf, 2012. Developmental rate: a unifying mechanism for sympatric divergence in postglacial fishes? Current Zoology 58: 21–34.

    Article  Google Scholar 

  • Merilä, J. & A. P. Hendry, 2014. Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evolutionary Applications 7: 1–14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Muir, A. M., P. Vecsei, T. C. Pratt, C. C. Krueger, M. Power & J. D. Reist, 2013. Ontogenetic shifts in morphology and resource use of cisco Coregonus artedi. Journal of Fish Biology 82: 600–617.

    Article  CAS  PubMed  Google Scholar 

  • Muir, A. M., M. T. Arts, M. A. Koops, T. B. Johnson, C. C. Krueger, T. M. Sutton & J. Rosenfeld, 2014. Reproductive life-history strategies in lake whitefish (Coregonus clupeaformis) from the Laurentian Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 71: 1256–1269.

    Article  CAS  Google Scholar 

  • Müller, R., 1992. Trophic state and its implications for natural reproduction of salmonid fish. Hydrobiologia 243: 261–268.

    Article  Google Scholar 

  • Myers, R. A., N. J. Barrowman, J. A. Hutchings, A. A. Rosenberg. (1995) Population dynamics of exploited fish stocks at low population levels. Science 269(5227): 1106–1108.

    Article  CAS  PubMed  Google Scholar 

  • Myers, J. T., D. L. Yule, M. L. Jones, T. D. Ahrenstorff, T. R. Hrabik, R. M. Claramunt, M. P. Ebener & E. K. Berglund, 2015. Spatial synchrony in cisco recruitment. Fisheries Research 165: 11–21.

    Article  Google Scholar 

  • Nagler, J. J., J. E. Parsons & J. G. Cloud, 2000. Single pair mating indicates maternal effects on embryo survival in rainbow trout, Oncorhynchus mykiss. Aquaculture 184: 177–183.

    Article  Google Scholar 

  • Narum, S. R., N. R. Campbell, K. A. Meyer, M. R. Miller & R. W. Hardy, 2013. Thermal adaptation and acclimation of ectotherms from differing aquatic climates. Molecular Ecology 22: 3090–3097.

    Article  PubMed  Google Scholar 

  • Neff, B. D. & T. E. Pitcher, 2005. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Molecular Ecology 14: 19–38.

    Article  CAS  PubMed  Google Scholar 

  • Nyberg, P., E. Bergstrand, E. Degerman & O. Enderlein, 2001. Recruitment of pelagic fish in an unstable climate: studies in Sweden’s four largest lakes. Ambio 30: 559–564.

    Article  CAS  PubMed  Google Scholar 

  • O’Reilly, C. M., R. J. Rowley, P. Schneider, J. D. Lenters, P. B. Mcintyre & B. M. Kraemer, 2015. Rapid and highly variable warming of lake surface waters around the globe. Geophysical Research Letters 42: 1–9.

    Google Scholar 

  • Oberlercher, T. M. & J. Wanzenböck, 2016. Impact of electric fishing on egg survival of whitefish, Coregonus lavaretus. Fisheries Management and Ecology 23: 540–547.

    Article  Google Scholar 

  • Ohlberger, J., G. Staaks & F. Hölker, 2007. Effects of temperature, swimming speed and body mass on standard and active metabolic rate in vendace (Coregonus albula). Journal of Comparative Physiology 177: 905–916.

    Article  PubMed  Google Scholar 

  • Ohlberger, J., T. Mehner, G. Staaks & F. Hölker, 2008. Is ecological segregation in a pair of sympatric coregonines supported by divergent feeding efficiencies? Canadian Journal of Fisheries and Aquatic Sciences 65: 2105–2113.

    Article  Google Scholar 

  • Oomen, R. A. & J. A. Hutchings, 2015. Variation in spawning time promotes genetic variability in population responses to environmental change in a marine fish. Conservation Physiology 3: 1–12.

    Article  CAS  Google Scholar 

  • Pariseau, R., P. Dumont & J.-G. Migneault, 1983. Découverte, dans le sud-ouest du Québec, d’une population de cisco de lac, Coregonus artedii, frayant au printemps. Canadian Journal of Zoology 61: 2365–2368.

    Article  Google Scholar 

  • Paufve, M. R., 2019. Diversity in spawning habitat across Great Lakes Cisco populations [Master’s thesis]. Cornell University.

  • Pauly, D. & R. S. V. Pullin, 1988. Hatching time in spherical, pelagic, marine fish eggs in response to temperature and egg size. Environmental Biology of Fishes 22: 261–271.

    Article  Google Scholar 

  • Pepin, P., 1991. Effect of temperature and size on development, mortality, and survival rates of the pelagic early life history stages of marine fish. Canadian Journal of Fisheries and Aquatic Sciences 48: 503–518.

    Article  Google Scholar 

  • Pritchard, A. L., 1931. Spawning habits and fry of the cisco (Leucichthys artedi) in Lake Ontario. Contributions to Canadian Biology and Fisheries 6: 225–240.

    Article  Google Scholar 

  • R Core Team, 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.r-project.org/.

  • Reist, J. D., F. J. Wrona, T. D. Prowse, M. Power, J. B. Dempson, R. J. Beamish, J. R. King, T. J. Carmichael & C. D. Sawatzky, 2006. General effects of climate change on Arctic fishes and fish populations. AMBIO: A Journal of the Human Environment 35: 370–380.

    Article  Google Scholar 

  • Schindler, D. E., J. B. Armstrong, & T. E. Reed (2015) The portfolio concept in ecology and evolution. Frontiers in Ecology and the Environment 13(5): 257-263.

    Article  Google Scholar 

  • Schindler, D. W., K. G. Beaty, E. J. Fee, D. R. Cruikshank, E. R. DeBruyn, D. L. Findlay, G. A. Linsey, J. A. Shearer, M. P. Stainton & M. A. Turner, 1990. Effects of climatic warming on lakes of the Central Boreal Forest. Science 250: 967–970.

    Article  CAS  PubMed  Google Scholar 

  • Schindler, D. E., R. Hilborn, B. Chasco, C. P. Boatright, T. P. Quinn, L. A. Rogers & M. S. Webster, 2010. Population diversity and the portfolio effect in an exploited species. Nature 465: 609–612.

    Article  CAS  PubMed  Google Scholar 

  • Schmitt, J. D., C. S. Vandergoot, B. P. O’Malley & R. T. Kraus, 2020. Does Lake Erie still have sufficient oxythermal habitat for cisco Coregonus artedi? Journal of Great Lakes Research 46: 330–338.

    Article  CAS  Google Scholar 

  • Schultz, E. T., K. E. Reynolds & D. O. Conover, 1996. Countergradient variation in growth among newly Hatched Fundulus heteroclitus: geographic differences revealed by common-environment experiments. Functional Ecology 10: 366.

    Article  Google Scholar 

  • Schultz, E. T., D. O. Conover & A. Ehtisham, 1998. The dead of winter: size-dependent variation and genetic differences in seasonal mortality among Atlantic silverside (Atherinidae: Menidia menidia) from different latitudes. Canadian Journal of Fisheries and Aquatic Sciences 55: 1149–1157.

    Article  Google Scholar 

  • Schulz, M. & J. Freyhof, 2003. Coregonus fontanae, a new spring-spawning cisco from Lake Stechlin, northern Germany (Salmoniformes: Coregonidae). Ichthyological Exploration of Freshwaters 14: 209–216.

    Google Scholar 

  • Schulz, M., J. Freyhof, R. Saint-Laurent, K. Østbye, T. Mehner, L. Bernatchez, R. Saint-Laurent, K. Østbye, T. Mehner & L. Bernatchez, 2006. Evidence for independent origin of two spring-spawning ciscoes (Salmoniformes: Coregonidae) in Germany. Journal of Fish Biology 68: 119–135.

    Article  CAS  Google Scholar 

  • Scott, W. B., & E. J. Crossman, 1973. Freshwater Fishes of Canada. Bulletin 184. Fisheries Research Board of Canada.

  • Sharma, S., K. Blagrave, J. J. Magnuson, C. M. O’Reilly, S. Oliver, R. D. Batt, M. R. Magee, D. Straile, G. A. Weyhenmeyer & L. A. Winslow, 2019. Widespread loss of lake ice around the Northern Hemisphere in a warming world. Nature Climate Change 9: 227.

    Article  Google Scholar 

  • Sharma, S., M. F. Meyer, J. Culpepper, X. Yang, S. E. Hampton, S. A. Berger, M. R. Brousil, S. C. Fradkin, S. N. Higgins & K. J. Jankowski, 2020. Integrating perspectives to understand lake ice dynamics in a changing world. Journal of Geophysical Research: Biogeosciences 125: 1–18.

    Google Scholar 

  • Siikavoipio, S. I., R. Knudsen, P. A. Amundsen, B. S. Sæther & P. James, 2012. Effects of high temperature on the growth of European whitefish (Coregonus lavaretus L.). Aquaculture Research 44: 8–12.

    Article  Google Scholar 

  • Sipponen, M., K. Muje, T. J. Marjomäki, P. Valkeajärvi & J. Karjalainen, 2006. Interlocked use of inland fish resources: a new management strategy under private property rights. Fisheries Management and Ecology 13: 299–307.

    Article  Google Scholar 

  • Somero, G. N., 2010. The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. Journal of Experimental Biology 213: 912–920.

    Article  CAS  PubMed  Google Scholar 

  • Stockwell, J. D., M. P. Ebener, J. A. Black, O. T. Gorman, T. R. Hrabik, R. E. Kinnunen, W. P. Mattes, J. K. Oyadomari, S. T. Schram, D. R. Schreiner, M. J. Seider, S. P. Sitar & D. L. Yule, 2009. A synthesis of cisco recovery in Lake Superior: implications for native fish rehabilitation in the Laurentian Great Lakes. North American Journal of Fisheries Management 29: 626–652.

    Article  Google Scholar 

  • Tapaninen, M., T. J. Marjomäki & T. Keskinen, 1998. The seasonal final temperature preferenda of immature vendace, Coregonus albula (L.). Archiv für Hydrobiologie 50: 131–141.

    Google Scholar 

  • Urpanen, O., H. Huuskonen, T. J. Marjomäki & J. Karjalainen, 2005. Growth and size-selective mortality of vendace (Coregonus albula (L.)) and whitefish (C. lavaretus L.) larvae. Boreal Environment Research 10: 225–238.

    Google Scholar 

  • van Damme, C. J. G., M. Dickey-Collas, A. D. Rijnsdorp & O. S. Kjesbu, 2009. Fecundity, atresia, and spawning strategies of Atlantic herring (Clupea harengus). Canadian Journal of Fisheries & Aquatic Sciences 66: 2130–2141.

    Article  Google Scholar 

  • Vielma, J., J. Koskela & K. Ruohonen, 2002. Growth, bone mineralization, and heat and low oxygen tolerance in European whitefish (Coregonus lavaretus L.) fed with graded levels of phosphorus. Aquaculture 212: 321–333.

    Article  CAS  Google Scholar 

  • Voeten, C. C., 2020. buildmer: Stepwise Elimination and Term Reordering for Mixed-Effects Regression., https://cran.r-project.org/package=buildmer.

  • Vonlanthen, P., D. Roy, A. G. Hudson, C. R. Largiadèr, D. Bittner & O. Seehausen, 2009. Divergence along a steep ecological gradient in lake whitefish (Coregonus sp.). Journal of Evolutionary Biology 22: 498–514.

    Article  CAS  PubMed  Google Scholar 

  • Vonlanthen, P., D. Bittner, A. G. Hudson, K. A. Young, R. Müller, B. Lundsgaard-Hansen, D. Roy, S. Di Piazza, C. R. Largiader, O. Seehausen, C. R. Largiadèr & O. Seehausen, 2012. Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482: 357–362.

    Article  CAS  PubMed  Google Scholar 

  • Vörösmarty, C. J., P. B. McIntyre, M. O. Gessner, D. Dudgeon, A. Prusevich, P. Green, S. Glidden, S. E. Bunn, C. A. Sullivan & C. R. Liermann, 2010. Global threats to human water security and river biodiversity. Nature 467: 555–561.

    Article  PubMed  CAS  Google Scholar 

  • Wedekind, C., G. Evanno, D. Urbach, A. Jacob & R. Müller, 2008. ‘Good-genes’ and ‘compatible-genes’ effects in an Alpine whitefish and the information content of breeding tubercles over the course of the spawning season. Genetica 132: 199–208.

    Article  PubMed  Google Scholar 

  • White, C. R., L. A. Alton & P. B. Frappell, 2012. Metabolic cold adaptation in fishes occurs at the level of whole animal, mitochondria and enzyme. Proceedings of the Royal Society B: Biological Sciences 279: 1740–1747.

    Article  CAS  PubMed  Google Scholar 

  • Wilder, A. P., S. R. Palumbi, D. O. Conover & N. O. Therkildsen, 2020. Footprints of local adaptation span hundreds of linked genes in the Atlantic silverside genome. Evolution Letters 4: 430–443.

    Article  PubMed  PubMed Central  Google Scholar 

  • Winslow, L. A., J. S. Read, G. J. A. Hansen, K. C. Rose & D. M. Robertson, 2017. Seasonality of change: summer warming rates do not fully represent effects of climate change on lake temperatures. Limnology and Oceanography 62: 2168–2178.

    Article  Google Scholar 

  • Woolsey, E. S., S. A. Keith, M. Byrne, S. Schmidt-Roach & A. H. Baird, 2015. Latitudinal variation in thermal tolerance thresholds of early life stages of corals. Coral Reefs 34: 471–478.

    Article  Google Scholar 

  • Woolway, R. I., B. M. Kraemer, J. D. Lenters, C. J. Merchant, C. M. O’Reilly, & S. Sharma, 2020. Global lake responses to climate change. Nature Reviews Earth & Environment 1: 388–403.

  • Woolway, R. I., M. T. Dokulil, W. Marszelewski, M. Schmid, D. Bouffard & C. J. Merchant, 2017. Warming of Central European lakes and their response to the 1980s climate regime shift. Climatic Change 142: 505–520.

    Article  Google Scholar 

  • Wright, P. J. & E. A. Trippel, 2009. Fishery-induced demographic changes in the timing of spawning: consequences for reproductive success. Fish and Fisheries 10: 283–304.

    Article  Google Scholar 

  • Yamahira, K. & D. O. Conover, 2002. Intra- vs. Interspecific Latitudinal Variation in Growth: adaptation to Temperature or Seasonality? Ecology 83: 1252–1262.

    Article  Google Scholar 

  • Yule, D. L., S. A. Moore, M. P. Ebener, R. M. Claramunt, T. C. Pratt, L. L. Salawater & M. J. Connerton, 2013. Morphometric variation among spawning cisco aggregations in the Laurentian Great Lakes: are historic forms still present. Advances in Limnology 64: 119–132.

    Article  Google Scholar 

  • Zimmerman, M. S. & C. C. Krueger, 2009. An ecosystem perspective on re-establishing native deepwater fishes in the Laurentian Great Lakes. North American Journal of Fisheries Management 29: 1352–1371.

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Wisconsin Department of Natural Resources Bayfield Fisheries Field Station, U. S. Geological Survey (USGS) Tunison Laboratory of Aquatic Science, New York State Department of Environmental Conservation Cape Vincent Fisheries Station, and Konnevesi Research Station and local fishers for conducting field collections of spawning adults. We also thank Rachel Taylor, Mark Vinson, Daniel Yule, Caroline Rosinski, Jonna Kuha, and Rosanna Sjövik for help with fertilizations and experiment maintenance. This work was funded by the USGS under Grant/Cooperative Agreement No. G16AP00087 to the Vermont Water Resources and Lakes Studies Center and G17AC00042 to the University of Vermont. This work was made possible with funds made available to Lake Champlain by Senator Patrick Leahy through the Great Lakes Fishery Commission. We acknowledge INRAE, French National Research Institute for Agriculture, Food, and Environment, the UMR CARRTEL (INRAE - USMB) and the National Science Foundation (award number 1829451) for supporting a workshop to develop this experiment.

Funding

This study was funded by the United States Geological Survey under Grant/Cooperative Agreement No. G16AP00087 to the Vermont Water Resources and Lakes Studies Center and G17AC00042 to the University of Vermont. This work was made possible with funds made available to Lake Champlain by Senator Patrick Leahy through the Great Lakes Fishery Commission. A workshop to develop this experiment was supported by INRAE, French National Research Institute for Agriculture, Food, and Environment, the UMR CARRTEL (INRAE - USMB), and the National Science Foundation (award number 1829451).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation and data collection were performed by Taylor R. Stewart (TS) and Mikko Mäkinen. Analysis was performed by TS. The first draft of the manuscript was written by TS and all authors commented on subsequent versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Taylor R. Stewart.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

All work described here was approved for ethical animal care under University of Vermont’s Institutional Animal Care and Use Committee (Protocol # PROTO202000021).

Additional information

Handling editor: Eric R. Larson.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 152 kb)

Supplementary material 2 (PDF 131 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stewart, T.R., Mäkinen, M., Goulon, C. et al. Influence of warming temperatures on coregonine embryogenesis within and among species. Hydrobiologia 848, 4363–4385 (2021). https://doi.org/10.1007/s10750-021-04648-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-021-04648-0

Keywords

Navigation