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Embryonic critical windows: changes in incubation temperature alter survival, hatchling phenotype, and cost of development in lake whitefish (Coregonus clupeaformis)

Abstract

The timing, success and energetics of fish embryonic development are strongly influenced by temperature. However, it is unclear if there are developmental periods, or critical windows, when oxygen use, survival and hatchling phenotypic characteristics are particularly influenced by changes in the thermal environment. Therefore, we examined the effects of constant incubation temperature and thermal shifts on survival, hatchling phenotype, and cost of development in lake whitefish (Coregonus clupeaformis) embryos. We incubated whitefish embryos at control temperatures of 2, 5, or 8 °C, and shifted embryos across these three temperatures at the end of gastrulation or organogenesis. We assessed hatch timing, mass at hatch, and yolk conversion efficiency (YCE). We determined cost of development, the amount of oxygen required to build a unit of mass, for the periods from fertilization–organogenesis, organogenesis–fin flutter, fin flutter–hatch, and for total development. An increase in incubation temperature decreased time to 50 % hatch (164 days at 2 °C, 104 days at 5 °C, and 63 days at 8 °C), survival decreased from 55 % at 2 °C, to 38 % at 5 °C, and 17 % at 8 °C, and hatchling yolk-free dry mass decreased from 1.27 mg at 2 °C to 0.61 mg at 8 °C. Thermal shifts altered time to 50 % hatch and hatchling yolk-free dry mass and revealed a critical window during gastrulation in which a temperature change reduced survival. YCE decreased and cost of development increased with increased incubation temperature, but embryos that hatched at 8 °C and were incubated at colder temperatures during fertilization–organogenesis had reduced cost. The relationship between cost of development and temperature was altered during fin flutter–hatch, indicating it may be a critical window during which temperature has the greatest impact on energetic processes. The increase in cost of development with an increase in temperature has not been documented in other fishes and suggests whitefish embryos are more energy efficient at colder temperatures.

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Acknowledgments

We thank Chris Thome for help acquiring whitefish embryos, Abigail Lee for help monitoring hatching, the Ontario Ministry of Natural Resources for the permit to collect whitefish (UGLMU2013-08) and anonymous reviewers for their helpful comments. C.A.M. and J.E. were supported by a MITACS Accelerate grant to D.R.B. and J.Y.W. Funding was provided by Bruce Power and a Collaborative Research and Development Grant from the Natural Sciences and Engineering Research Council of Canada to J.Y.W., R.G.M., and C.M.S.

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Correspondence to Casey A. Mueller.

Additional information

Communicated by H.V. Carey.

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Mueller, C.A., Eme, J., Manzon, R.G. et al. Embryonic critical windows: changes in incubation temperature alter survival, hatchling phenotype, and cost of development in lake whitefish (Coregonus clupeaformis). J Comp Physiol B 185, 315–331 (2015). https://doi.org/10.1007/s00360-015-0886-8

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Keywords

  • Cost of development
  • Critical window
  • Growth
  • Embryonic fish
  • Survival
  • Temperature