Journal of Comparative Physiology B

, Volume 185, Issue 3, pp 315–331 | Cite as

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

  • Casey A. Mueller
  • John Eme
  • Richard G. Manzon
  • Christopher M. Somers
  • Douglas R. Boreham
  • Joanna Y. Wilson
Original Paper

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.

Keywords

Cost of development Critical window Growth Embryonic fish Survival Temperature 

References

  1. Bagarinao T (1986) Yolk resorption, onset of feeding and survival potential of larvae of three tropical marine fish species reared in the hatchery. Mar Biol 91:449–459CrossRefGoogle Scholar
  2. Beers Y (1953) Introduction to the theory of error. Addison-Wesley Publishing Company Inc, CambridgeGoogle Scholar
  3. Brooke LT (1975) Effect of different constant incubation temperatures on egg survival and embryonic development in Lake whitefish (Coregonus clupeaformis). Trans Am Fish Soc 104:555–559CrossRefGoogle Scholar
  4. Burggren WW (1998) Studying physiological development: past, present and future. Biol Bull 33:71–84Google Scholar
  5. Burggren WW, Reyna KS (2011) Developmental trajectories, critical windows and phenotypic alteration during cardio-respiratory development. Resp Physiol Neurobiol 178:13–21CrossRefGoogle Scholar
  6. Das T, Pal AK, Chakraborty SK, Manush SM, Dalvi RS, Sarma K, Mukherjee SC (2006) Thermal dependence of embryonic development and hatching rate in Labeo rohita (Hamilton, 1822). Aquaculture 255:536–541CrossRefGoogle Scholar
  7. Eme J, Mueller CA, Manzon RG, Somers CM, Boreham DR, Wilson JY (2015) Critical windows in embryonic development: shifting incubation temperatures alter heart rate and oxygen consumption of Lake Whitefish (Coregonus clupeaformis) embryos and hatchlings. Comp Biochem Physiol A 179:71–80CrossRefGoogle Scholar
  8. Ficke AD, Myrick CA, Hansen LJ (2007) Potential impacts of global climate change on freshwater fisheries. Rev Fish Biol Fisher 17:581–613CrossRefGoogle Scholar
  9. Finn RN, Fyhn HJ, Evjen MS (1991) Respiration and nitrogen metabolism of Atlantic halibut eggs (Hippoglossus hippoglossus). Mar Biol 108:11–19CrossRefGoogle Scholar
  10. Finn RN, Fyhn HJ, Evjen MS (1995a) Physiological energetics of developing embryos and yolk-sec larvae of Atlantic cod (Gadus morhua) I. Respiration and nitrogen metabolism. Mar Biol 124:355–369CrossRefGoogle Scholar
  11. Finn RN, Rønnestad I, Fyhn HJ (1995b) Respiration, nitrogen and energy metabolism of developing yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus L.). Comp Biochem Physiol A 111:647–671CrossRefGoogle Scholar
  12. Gruber K, Wieser W (1983) Energetics of development of the alpine charr, Salvelinus alpinus, in relation to temperature and oxygen. J Comp Physiol B 149:485–493CrossRefGoogle Scholar
  13. Hamor T, Garside ET (1977) Size relations and yolk utilization in embryonated ova and alevins of Atlantic salmon Salmo salar L. in various combinations of temperature and dissolved oxygen. Can J Zool 55:1892–1898CrossRefPubMedGoogle Scholar
  14. Heming T (1982) Effects of temperature on utilization of yolk by chinook salmon (Oncorhynchus tshawytscha) eggs and alevins. Can J Fish Aquat Sci 39:184–190CrossRefGoogle Scholar
  15. Herzig A, Winkler H (1986) The influence of temperature on the embryonic development of three cyprinid fishes, Abramis brama, Chalcalburnus chalcoides mento and Vimba vimba. J Fish Biol 28:171–181CrossRefGoogle Scholar
  16. Kamler E (2008) Resource allocation in yolk-feeding fish. Rev Fish Biol Fisher 18:143–200CrossRefGoogle Scholar
  17. Kamler E, Keckeis H, Bauer-Nemeschkal E (1998) Temperature-induced changes of survival, development and yolk partitioning in Chondrostoma nasus. J Fish Biol 53:658–682Google Scholar
  18. Kinne O, Kinne EM (1962) Rates of development in embryos of a cyprinodont fish exposed to different temperature–salinity–oxygen combinations. Can J Zool 40:231–253CrossRefGoogle Scholar
  19. Lukšienė D, Sandström O, Lounasheimo L, Andersson J (2000) The effects of thermal effluent exposure on the gametogenesis of female fish. J Fish Biol 56:37–50CrossRefGoogle Scholar
  20. Macqueen DJ, Robb DH, Olsen T, Melstveit L, Paxton CG, Johnston IA (2008) Temperature until the ‘eyed stage’of embryogenesis programmes the growth trajectory and muscle phenotype of adult Atlantic salmon. Biol Lett 4:294–298CrossRefPubMedCentralPubMedGoogle Scholar
  21. Martell DJ, Kieffer JD, Trippel EA (2005) Effects of temperature during early life history on embryonic and larval development and growth in haddock. J Fish Biol 66:1558–1575CrossRefGoogle Scholar
  22. Mitz C, Thome C, Cybulski ME, Laframbo L, Somers CM, Manzon RG, Wilson JY, Boreham DR (2014) A self-contained, controlled hatchery system for rearing Lake whitefish embryos for experimental aquaculture. N Am J Aquacult 76(3):179–184CrossRefGoogle Scholar
  23. Mueller CA, Augustine S, Kooijman SALM, Kearney MR, Seymour RS (2012) The trade-off between maturation and growth during accelerated development in frogs. Comp Biochem Physiol A 163:95–102CrossRefGoogle Scholar
  24. Mueller CA, Joss JMP, Seymour RS (2011) The energy cost of embryonic development in fishes and amphibians, with emphasis on new data from the Australian lungfish, Neoceratodus forsteri. J Comp Physiol B 181:43–52CrossRefPubMedGoogle Scholar
  25. Patrick PH, Chen E, Parks J, Powell J, Poulton J, Fietsch C-L (2013) Effects of fixed and fluctuating temperature on hatch of Round Whitefish and Lake Whitefish eggs. N Am J Fish Manag 33:1091–1099CrossRefGoogle Scholar
  26. Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367CrossRefPubMedGoogle Scholar
  27. Porter SM, Bailey KM (2007) The effect of early and late hatching on the escape response of walleye pollock (Theragra chalcogramma) larvae. J Plankton Res 29:291–300CrossRefGoogle Scholar
  28. Precht H (1958) Concepts of the temperature adaptation of unchanging reaction systems of cold-blooded animals. Physiological Adaptation. American Physiological Society, Washington, D.C.Google Scholar
  29. Price JW (1934a) The embryology of the whitefish Coregonus Clupeaformis, (Mitchill). Part I. Ohio J Sci 34:287–305Google Scholar
  30. Price JW (1934b) The embryology of the whitefish Coregonus Clupeaformis, (Mitchill). Part II. organogenesis. Ohio J Sci 34:399–414Google Scholar
  31. Price JW (1935) The embryology of the whitefish Coregonus Clupeaformis, (Mitchill). Part III. The second half of the incubation period. Ohio J Sci 35:40–53Google Scholar
  32. Price JW (1940) Time-temperature relations in the incubation of the whitefish, Coregonus clupeaformis (Mitchill). J Gen Physiol 23:449–468CrossRefPubMedCentralPubMedGoogle Scholar
  33. Rana K (1990) Influence of incubation temperature on Oreochromis niloticus (L.) eggs and fry: II. Survival, growth and feeding of fry developing solely on their yolk reserves. Aquaculture 87:183–195CrossRefGoogle Scholar
  34. Rombough PJ (1988) Growth, aerobic metabolism, and dissolved oxygen requirements of embryos and alevins of steelhead, Salmo gairdneri. Can J Zool 66:651–660CrossRefGoogle Scholar
  35. Rombough PJ (1994) Energy partitioning during fish development: additive or compensatory allocation of energy to support growth? Funct Ecol 8:178–186CrossRefGoogle Scholar
  36. Schnurr ME, Yin Y, Scott GR (2014) Temperature during embryonic development has persistent effects on metabolic enzymes in the muscle of zebrafish. J Exp Biol 217:1370–1380CrossRefPubMedGoogle Scholar
  37. Sreetharan S, Thome C, Mitz C, Eme J, Mueller CA, Hulley EN, Manzon RG, Somers CM, Boreham DR, Wilson JY (2015) Embryonic development of lake whitefish (Coregonus clupeaformis): a staging series, analysis of growth and impacts of fixation. J Fish Biol (in review)Google Scholar
  38. Vleck CM, Hoyt DF (1991) Metabolism and energetics of reptilian and avian embryos. In: Deeming DC, Ferguson MWJ (eds) Egg incubation: its effect on embryonic development in birds and reptiles. Cambridge University Press, Cambridge, pp 285–306CrossRefGoogle Scholar
  39. Vleck CM, Vleck D (1987) Metabolism and energetics of avian embryos. J Exp Zool Suppl 1:111–125PubMedGoogle Scholar
  40. Wieser W (1991) Limitations of energy acquisition and energy use in small poikilotherms: evolutionary implications. Funct Ecol 5:234–240CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Casey A. Mueller
    • 1
  • John Eme
    • 1
  • Richard G. Manzon
    • 2
  • Christopher M. Somers
    • 2
  • Douglas R. Boreham
    • 3
    • 4
    • 5
  • Joanna Y. Wilson
    • 1
  1. 1.Department of BiologyMcMaster UniversityHamiltonCanada
  2. 2.Department of BiologyUniversity of ReginaReginaCanada
  3. 3.Medical Sciences, Northern Ontario School of MedicineLaurentian UniversitySudburyCanada
  4. 4.Bruce PowerTivertonCanada
  5. 5.Department of Medical Physics and Applied Radiation SciencesMcMaster UniversityHamiltonCanada

Personalised recommendations